Comparative genomics of parallel in repeated adaptive radiations (GenAdap)

Institutionen
  • FB Biologie
Publikationen
  Bertinetti Cerrato, Cesar; Härer, Andreas; Karagic, Nidal; Meyer, Axel; Torres-Dowdall, Julián (2024): Repeated Divergence in Opsin Genes Expression Mirrors Photic Habitat Changes in Rapidly Evolving Crater Lake Cichlid Fishes The American Naturalist. University of Chicago Press. 2024, 203(5), pp. 604-617. ISSN 0003-0147. eISSN 1537-5323. Available under: doi: 10.1086/729420

Repeated Divergence in Opsin Genes Expression Mirrors Photic Habitat Changes in Rapidly Evolving Crater Lake Cichlid Fishes

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Selection pressures differ along environmental gradients and traits tightly linked to fitness (e.g., the visual system) are expected to track such variation. Along gradients, adaptation to local conditions might be due to heritable and non-heritable, environmentally induced variation. Disentangling these sources of phenotypic variation requires studying closely related populations in nature and the laboratory. The Nicaraguan lakes represent an environmental gradient in photic conditions from clear crater lakes to very turbid great lakes. From two old, turbid great lakes, Midas cichlid fish (Amphilophus cf. citrinellus) independently colonized seven isolated crater lakes of varying light conditions, resulting in a small adaptive radiation. We estimated visual sensitivities variation along this photic gradient by measuring cone opsin gene expression among lake populations. Visual sensitivities observed in all seven derived crater lake populations shifted predictably in direction and magnitude, repeatedly mirroring changes in photic conditions. Comparing wild-caught and laboratory-reared fish revealed that 48% of this phenotypic variation is genetically determined and evolved rapidly. Decreasing intrapopulation variation as environments become spectrally narrower suggests that different selective landscapes operate along the gradient. We conclude that the power to predict phenotypic evolution along gradients depends on both the magnitude of environmental change and the selective landscape shape.

Forschungszusammenhang (Projekte)

    Olave, Melisa; Griotti, Mariana; Carrara, Roldolfo; Franchini, Paolo; Meyer, Axel; Roig-Juñent, Sergio A. (2023): Historical Climate Change Dynamics Facilitated Speciation and Hybridization Between Highland and Lowland Species of Baripus Ground Beetles From Patagonia Bulletin of the Society of Systematic Biologists. The Ohio State University Libraries. 2023, 2(3), pp. 1-16. eISSN 2768-0819. Available under: doi: 10.18061/bssb.v2i3.9263

Historical Climate Change Dynamics Facilitated Speciation and Hybridization Between Highland and Lowland Species of Baripus Ground Beetles From Patagonia

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One of the largest beetles of Patagonia, Baripus (Cardiophthalmus), includes 20 currently described species. Its distribution ranges from the tip of Patagonia, on Tierra del Fuego Island, to isolated patches along the Andes and extra-Andes mountains in northern Patagonia on the Payunia at >3000 m elevation. Here, using RADseq data, evidence is found of mixed ancestry in different lineages. Phylogenetic network reconstruction shows two hybridizing edges between lowland and highland species. Using environmental niche modeling, we show changes in geographic distribution of potential niches of species during the last glacial maximum compared to their present distribution. Increasing potential niche overlap among different species pairs possibly explains how lineages came into secondary contact, supporting the hypothesis of hybridization. In addition, morphological evolution is studied using geometric morphometrics on the network, and evidence of transgressive evolution has been found involving the pronotum shape, as well as highland/lowland habitat preferences. Finally, based on genomics and morphological data and using an integrative coalescent-based species delimitation approach, the separate evolution of two lineages in early stages of speciation is found. Taken together, dynamics of diversification of Baripus beetles in both space and time are discussed.

Forschungszusammenhang (Projekte)

    Kratochwil, Claudius F.; Kautt, Andreas F.; Rometsch, Sina J.; Meyer, Axel (2022): Benefits and limitations of a new genome‐based PCR‐RFLP genotyping assay (GB‐RFLP) : A SNP‐based detection method for identification of species in extremely young adaptive radiations Ecology and Evolution. Wiley. 2022, 12(3), e8751. eISSN 2045-7758. Available under: doi: 10.1002/ece3.8751

Benefits and limitations of a new genome‐based PCR‐RFLP genotyping assay (GB‐RFLP) : A SNP‐based detection method for identification of species in extremely young adaptive radiations

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High-throughput DNA sequencing technologies make it possible now to sequence entire genomes relatively easily. Complete genomic information obtained by whole-genome resequencing (WGS) can aid in identifying and delineating species even if they are extremely young, cryptic, or morphologically difficult to discern and closely related. Yet, for taxonomic or conservation biology purposes, WGS can remain cost-prohibitive, too time-consuming, and often constitute a “data overkill.” Rapid and reliable identification of species (and populations) that is also cost-effective is made possible by species-specific markers that can be discovered by WGS. Based on WGS data, we designed a PCR restriction fragment length polymorphism (PCR-RFLP) assay for 19 Neotropical Midas cichlid populations (Amphilophus cf. citrinellus), that includes all 13 described species of this species complex. Our work illustrates that identification of species and populations (i.e., fish from different lakes) can be greatly improved by designing genetic markers using available “high resolution” genomic information. Yet, our work also shows that even in the best-case scenario, when whole-genome resequencing information is available, unequivocal assignments remain challenging when species or populations diverged very recently, or gene flow persists. In summary, we provide a comprehensive workflow on how to design RFPL markers based on genome resequencing data, how to test and evaluate their reliability, and discuss the benefits and pitfalls of our approach.

Forschungszusammenhang (Projekte)

    Höch, Rebekka; Schneider, Ralf F.; Kickuth, Alison; Meyer, Axel; Woltering, Joost M. (2021): Spiny and soft-rayed fin domains in acanthomorph fish are established through a BMP-gremlin-shh signaling network Proceedings of the National Academy of Sciences of the United States of America. National Academy of Sciences. 2021, 118(29), e2101783118. ISSN 0027-8424. eISSN 1091-6490. Available under: doi: 10.1073/pnas.2101783118

Spiny and soft-rayed fin domains in acanthomorph fish are established through a BMP-gremlin-shh signaling network

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With over 18,000 species, the Acanthomorpha, or spiny-rayed fishes, form the largest and arguably most diverse radiation of vertebrates. One of the key novelties that contributed to their evolutionary success are the spiny rays in their fins that serve as a defense mechanism. We investigated the patterning mechanisms underlying the differentiation of median fin Anlagen into discrete spiny and soft-rayed domains during the ontogeny of the direct-developing cichlid fish Astatotilapia burtoni Distinct transcription factor signatures characterize these two fin domains, whereby mutually exclusive expression of hoxa13a/b with alx4a/b and tbx2b marks the spine to soft-ray boundary. The soft-ray domain is established by BMP inhibition via gremlin1b, which synergizes in the posterior fin with shh secreted from a zone of polarizing activity. Modulation of BMP signaling by chemical inhibition or gremlin1b CRISPR/Cas9 knockout induces homeotic transformations of spines into soft rays and vice versa. The expression of spine and soft-ray genes in nonacanthomorph fins indicates that a combination of exaptation and posterior expansion of an ancestral developmental program for the anterior fin margin allowed the evolution of robustly individuated spiny and soft-rayed domains. We propose that a repeated exaptation of such pattern might underly the convergent evolution of anterior spiny-fin elements across fishes.

Forschungszusammenhang (Projekte)

    Urban, Sabine; Nater, Alexander; Meyer, Axel; Kratochwil, Claudius F. (2021): Different sources of allelic variation drove repeated color pattern divergence in cichlid fishes Molecular Biology and Evolution. Oxford University Press (OUP). 2021, 38(2), pp. 465-477. ISSN 0737-4038. eISSN 1537-1719. Available under: doi: 10.1093/molbev/msaa237

Different sources of allelic variation drove repeated color pattern divergence in cichlid fishes

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The adaptive radiations of East African cichlid fish in the Great Lakes Victoria, Malawi, and Tanganyika are well known for their diversity and repeatedly evolved phenotypes. Convergent evolution of melanic horizontal stripes has been linked to a single locus harboring the gene agouti-related peptide 2 (agrp2). However, where and when the causal variants underlying this trait evolved and how they drove phenotypic divergence remained unknown. To test the alternative hypotheses of standing genetic variation versus de novo mutations (independently originating in each radiation), we searched for shared signals of genomic divergence at the agrp2 locus. While we discovered similar signatures of differentiation at the locus level, the haplotypes associated with stripe patterns are surprisingly different. In Lake Malawi, the highest associated alleles are located within and close to the 5' untranslated region of agrp2 and likely evolved through recent de novo mutations. In the younger Lake Victoria radiation, stripes are associated with two intronic regions overlapping with a previously reported cis-regulatory interval. The origin of these segregating haplotypes predates the Lake Victoria radiation since they are also found in more basal riverine and Lake Kivu species. This suggest that both segregating haplotypes were present as standing genetic variation at the onset of the Lake Victoria adaptive radiation with their more than 500 species and drove phenotypic divergence within the species flock. In summary, both new (Lake Malawi) or ancient (Lake Victoria) allelic variation at the same locus can fuel rapid and convergent phenotypic evolution.

Forschungszusammenhang (Projekte)

    Olave, Melisa; Meyer, Axel (2020): Implementing Large Genomic Single Nucleotide Polymorphism Data Sets in Phylogenetic Network Reconstructions : A Case Study of Particularly Rapid Radiations of Cichlid Fish Systematic Biology. Oxford University Press (OUP). 2020, 69(5), pp. 848-862. ISSN 1063-5157. eISSN 1076-836X. Available under: doi: 10.1093/sysbio/syaa005

Implementing Large Genomic Single Nucleotide Polymorphism Data Sets in Phylogenetic Network Reconstructions : A Case Study of Particularly Rapid Radiations of Cichlid Fish

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The Midas cichlids of the Amphilophus citrinellus spp. species complex from Nicaragua (13 species) are an extraordinary example of adaptive and rapid radiation (< 24,000 years old). These cichlids are a very challenging group to infer its evolutionary history in phylogenetic analyses, due to the apparent prevalence of incomplete lineage sorting (ILS), as well as past and current gene flow. Assuming solely a vertical transfer of genetic material from an ancestral lineage to new lineages is not appropriate in many cases of genes transferred horizontally in nature. Recently developed methods to infer phylogenetic networks under such circumstances might be able to circumvent these problems. These models accommodate not just ILS, but also gene flow, under the multispecies network coalescent model (MSNC), processes that are at work in young, hybridizing, and/or rapidly diversifying lineages. There are currently only a few programs available that implement MSNC for estimating phylogenetic networks. Here, we present a novel way to incorporate single nucleotide polymorphism (SNP) data into the currently available PhyloNetworks program. Based on simulations, we demonstrate that SNPs can provide enough power to recover the true phylogenetic network. We also show that it can accurately infer the true network more often than other similar SNP-based programs (PhyloNet and HyDe). Moreover, our approach results in a faster algorithm compared to the original pipeline in PhyloNetworks, without losing power. We also applied our new approach to infer the phylogenetic network of Midas cichlid radiation. We implemented the most comprehensive genomic dataset to date (RADseq dataset of 679 individuals and >37K SNPs from 19 ingroup lineages) and present estimated phylogenetic networks for this extremely young and fast-evolving radiation of cichlid fish. We demonstrate that the MSNC is more appropriate than the multispecies coalescent alone for the analysis of this rapid radiation.

Forschungszusammenhang (Projekte)

    Woltering, Joost M.; Irisarri, Iker; Ericsson, Rolf; Joss, Jean M. P.; Sordino, Paolo; Meyer, Axel (2020): Sarcopterygian fin ontogeny elucidates the origin of hands with digits Science Advances. American Association for the Advancement of Science (AAAS). 2020, 6(34), eabc3510. eISSN 2375-2548. Available under: doi: 10.1126/sciadv.abc3510

Sarcopterygian fin ontogeny elucidates the origin of hands with digits

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How the hand and digits originated from fish fins during the Devonian fin-to-limb transition remains unsolved. Controversy in this conundrum stems from the scarcity of ontogenetic data from extant lobe-finned fishes. We report the patterning of an autopod-like domain by hoxa13 during fin development of the Australian lungfish, the most closely related extant fish relative of tetrapods. Differences from tetrapod limbs include the absence of digit-specific expansion of hoxd13 and hand2 and distal limitation of alx4 and pax9, which potentially evolved through an enhanced response to shh signaling in limbs. These developmental patterns indicate that the digit program originated in postaxial fin radials and later expanded anteriorly inside of a preexisting autopod-like domain during the evolution of limbs. Our findings provide a genetic framework for the transition of fins into limbs that supports the significance of classical models proposing a bending of the tetrapod metapterygial axis.

Forschungszusammenhang (Projekte)

    Torres-Dowdall, Julián; Rometsch, Sina J.; Kautt, Andreas F.; Aguilera, Gastón; Meyer, Axel (2020): The direction of genital asymmetry is expressed stochastically in internally fertilizing anablepid fishes Proceedings of the Royal Society of London, Series B : Biological Sciences. Royal Society of London. 2020, 287(1930), 20200969. ISSN 0962-8452. eISSN 1471-2954. Available under: doi: 10.1098/rspb.2020.0969

The direction of genital asymmetry is expressed stochastically in internally fertilizing anablepid fishes

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Animal genitalia vary considerably across taxa, with divergence in many morphological traits, including striking departures from symmetry. Different mechanisms have been proposed to explain this diversity, mostly assuming that at least some of the phenotypic variation is heritable. However, heritability of the direction of genital asymmetry has been rarely determined. Anablepidae are internally fertilizing fish where the anal fin of males has been modified into an intromittent organ that transfers sperm into the gonopore of females. Males of anablepid fishes exhibit asymmetric genitalia, and both left- and right-sided individuals are commonly found at similar proportions within populations (i.e. antisymmetry). Although this polymorphism was described over a century ago, there have been no attempts to determine if genital asymmetry has a genetic basis and whether the different morphs are accumulating genetic differences, as might be expected since in some species females have also asymmetric gonopores and thereby can only be fertilized by compatible asymmetric males. We address this issue by combining breeding experiments with genome-wide data (ddRAD markers) in representative species of the two anablepid genera with asymmetric genitalia: Anableps and Jenynsia. Breeding experiments showed that all offspring were asymmetric, but their morphotype (i.e. right- or left-sided) was independent of parental morphotype, implying that the direction of asymmetry does not have a strong genetic component. Consistent with this conclusion, association analyses based on approximately 25 000 SNPs did not identify markers significantly associated with the direction of genital asymmetry and there was no evidence of population structure between left- and right-sided individuals. These results suggest that the direction of genital asymmetry in anablepid fishes might be stochastic, a commonly observed pattern in species with antisymmetry in morphological traits.

Forschungszusammenhang (Projekte)

    Liang, Yipeng; Gerwin, Jan; Meyer, Axel; Kratochwil, Claudius F. (2020): Developmental and Cellular Basis of Vertical Bar Color Patterns in the East African Cichlid Fish Haplochromis latifasciatus Frontiers in Cell and Developmental Biology. Frontiers Media. 2020, 8, 62. eISSN 2296-634X. Available under: doi: 10.3389/fcell.2020.00062

Developmental and Cellular Basis of Vertical Bar Color Patterns in the East African Cichlid Fish Haplochromis latifasciatus

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The East African adaptive radiations of cichlid fishes are renowned for their diversity in coloration. Yet, the developmental basis of pigment pattern formation remains largely unknown. One of the most common melanic patterns in cichlid fishes are vertical bar patterns. Here we describe the ontogeny of this conspicuous pattern in the Lake Kyoga species Haplochromis latifasciatus. Beginning with the larval stages we tracked the formation of this stereotypic color pattern and discovered that its macroscopic appearance is largely explained by an increase in melanophore density and accumulation of melanin during the first 3 weeks post-fertilization. The embryonal analysis is complemented with cytological quantifications of pigment cells in adult scales and the dermis beneath the scales. In adults, melanic bars are characterized by a two to threefold higher density of melanophores than in the intervening yellow interbars. We found no strong support for differences in other pigment cell types such as xanthophores. Quantitative PCRs for twelve known pigmentation genes showed that expression of melanin synthesis genes tyr and tyrp1a is increased five to sixfold in melanic bars, while xanthophore and iridophore marker genes are not differentially expressed. In summary, we provide novel insights on how vertical bars, one of the most widespread vertebrate color patterns, are formed through dynamic control of melanophore density, melanin synthesis and melanosome dispersal.

Forschungszusammenhang (Projekte)

    Irisarri, Iker; Singh, Pooja; Koblmüller, Stephan; Torres-Dowdall, Julián; Henning, Frederico; Franchini, Paolo; Fischer, Christoph; Lemmon, Alan R.; Sturmbauer, Christian; Meyer, Axel (2018): Phylogenomics uncovers early hybridization and adaptive loci shaping the radiation of Lake Tanganyika cichlid fishes Nature communications. 2018, 9, 3159. eISSN 2041-1723. Available under: doi: 10.1038/s41467-018-05479-9

Phylogenomics uncovers early hybridization and adaptive loci shaping the radiation of Lake Tanganyika cichlid fishes

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Lake Tanganyika is the oldest and phenotypically most diverse of the three East African cichlid fish adaptive radiations. It is also the cradle for the younger parallel haplochromine cichlid radiations in Lakes Malawi and Victoria. Despite its evolutionary significance, the relationships among the main Lake Tanganyika lineages remained unresolved, as did the general timescale of cichlid evolution. Here, we disentangle the deep phylogenetic structure of the Lake Tanganyika radiation using anchored phylogenomics and uncover hybridization at its base, as well as early in the haplochromine radiation. This suggests that hybridization might have facilitated these speciation bursts. Time-calibrated trees support that the radiation of Tanganyika cichlids coincided with lake formation and that Gondwanan vicariance concurred with the earliest splits in the cichlid family tree. Genes linked to key innovations show signals of introgression or positive selection following colonization of lake habitats and species' dietary adaptations are revealed as major drivers of colour vision evolution. These findings shed light onto the processes shaping the evolution of adaptive radiations.

Forschungszusammenhang (Projekte)

    Härer, Andreas; Meyer, Axel; Torres-Dowdall, Julián (2018): Convergent phenotypic evolution of the visual system via different molecular routes : how Neotropical cichlid fishes adapt to novel light environments Evolution Letters. 2018, 2(4), pp. 341-354. eISSN 2056-3744. Available under: doi: 10.1002/evl3.71

Convergent phenotypic evolution of the visual system via different molecular routes : how Neotropical cichlid fishes adapt to novel light environments

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How predictable is evolution? This remains a fundamental but contested issue in evolutionary biology. When independent lineages colonize the same environment, we are presented with a natural experiment that allows us to ask if genetic and ecological differences promote species‐specific evolutionary outcomes or whether species phenotypically evolve in a convergent manner in response to shared selection pressures. If so, are the molecular mechanisms underlying phenotypic convergence the same? In Nicaragua, seven species of cichlid fishes concurrently colonized two novel photic environments. Hence, their visual system represents a compelling model to address these questions, particularly since the adaptive value of phenotypic changes is well‐understood. By analyzing retinal transcriptomes, we found that differential expression of genes responsible for color vision (cone opsins and cyp27c1) produced rapid and mostly convergent changes of predicted visual sensitivities. Notably, these changes occurred in the same direction in all species although there were differences in underlying gene expression patterns illustrating nonconvergence at the molecular level. Adaptive phenotypes evolved deterministically, even when species differ substantially in ecology and genetic variation. This provides strong evidence that phenotypic evolution of the visual system occurred in response to similar selective forces of the photic environment.

Forschungszusammenhang (Projekte)

    Kautt, Andreas F.; Machado-Schiaffino, Gonzalo; Meyer, Axel (2018): Lessons from a natural experiment : Allopatric morphological divergence and sympatric diversification in the Midas cichlid species complex are largely influenced by ecology in a deterministic way Evolution Letters. 2018, 2(4), pp. 323-340. eISSN 2056-3744. Available under: doi: 10.1002/evl3.64

Lessons from a natural experiment : Allopatric morphological divergence and sympatric diversification in the Midas cichlid species complex are largely influenced by ecology in a deterministic way

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Explaining why some lineages diversify while others do not and how are key objectives in evolutionary biology. Young radiations of closely related species derived from the same source population provide an excellent opportunity to disentangle the relative contributions of possible drivers of diversification. In these settings, lineage‐specific effects are shared and can be ruled out. Moreover, the relevant demographic and ecological parameters can be estimated accurately. Midas cichlid fish in Nicaragua have repeatedly colonized several crater lakes, diverged from the same source populations, and, interestingly, diversified in some of them but not others. Here, using the most comprehensive molecular and geometric morphometric data set on Midas cichlids to date (∼20,000 SNPs, 12 landmarks, ∼700 individuals), we aim to understand why and how crater lake populations diverge and why some of them are more prone to diversify in sympatry than others. Taking ancestor‐descendant relationships into account, we find that Midas cichlids diverged in parallel from their source population mostly—but not exclusively—by evolving more slender body shapes in all six investigated crater lakes. Admixture among crater lakes has possibly facilitated this process in one case, but overall, admixture and secondary waves of colonization cannot predict morphological divergence and intralacustrine diversification. Instead, morphological divergence is larger the more dissimilar a crater lake is compared to the source lake and happens rapidly after colonization followed by a slow‐down with time. Our data also provide some evidence that founder effects may positively contribute to divergence. The depth of a crater lake is positively associated with variation in body shapes (and number of species), presumably by providing more ecological opportunities. In conclusion, we find that parallel morphological divergence in allopatry and the propensity for diversification in sympatry across the entire Midas cichlid fish radiation is partly predictable and mostly driven by ecology.

Forschungszusammenhang (Projekte)

    Karagic, Nidal; Härer, Andreas; Meyer, Axel; Torres-Dowdall, Julián (2018): Heterochronic opsin expression due to early light deprivation results in drastically shifted visual sensitivity in a cichlid fish : Possible role of thyroid hormone signaling Journal of Experimental Zoology Part B : Molecular and Developmental Evolution (JEZ). 2018, 330(4), pp. 202-214. ISSN 1552-5007. eISSN 1552-5015. Available under: doi: 10.1002/jez.b.22806

Heterochronic opsin expression due to early light deprivation results in drastically shifted visual sensitivity in a cichlid fish : Possible role of thyroid hormone signaling

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During early ontogeny, visual opsin gene expression in cichlids is influenced by prevailing light regimen. Red light, for example, leads to an early switch from the expression of short‐wavelength sensitive to long‐wavelength sensitive opsins. Here, we address the influence of light deprivation on opsin expression. Individuals reared in constant darkness during the first 14 days post‐hatching (dph) showed a general developmental delay compared with fish reared under a 12:12 hr light–dark cycle (control group). Several characters including pigmentation patterns and eye development, appeared later in dark‐reared individuals. Quantitative real‐time PCR and fluorescent in situ hybridization at six time points during the 14 days period revealed that fish from the control group expressed opsin genes from 5 dph on and maintained a short‐wavelength sensitive phenotype (sws1, rh2b, and rh2a). Onset of opsin expression in dark‐reared Midas cichlids was delayed by 4 days and visual sensitivity rapidly progressed toward a long‐wavelength sensitive phenotype (sws2b, rh2a, and lws). Shifts in visual sensitivities toward longer wavelengths are mediated by thyroid hormone (TH) in many vertebrates. Compared to control fish, dark‐reared individuals showed elevated dio3 expression levels ‐ a validated proxy for TH concentration ‐ suggesting higher circulating TH levels. Despite decelerated overall development, ontogeny of opsin gene expression was accelerated, resulting in retinae with long‐wavelength shifted predicted sensitivities compared to light‐reared individuals. Indirect evidence suggests that this was due to altered TH metabolism.

Forschungszusammenhang (Projekte)

    Kratochwil, Claudius F.; Yipeng, Liang; Gerwin, Jan; Woltering, Joost M.; Urban, Sabine; Henning, Frederico; Machado-Schiaffino, Gonzalo; Hulsey, Christopher Darrin; Meyer, Axel (2018): Agouti-related peptide 2 facilitates convergent evolution of stripe patterns across cichlid fish radiations Science. 2018, 362(6413), pp. 457-460. ISSN 0036-8075. eISSN 1095-9203. Available under: doi: 10.1126/science.aao6809

Agouti-related peptide 2 facilitates convergent evolution of stripe patterns across cichlid fish radiations

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The color patterns of African cichlid fishes provide notable examples of phenotypic convergence. Across the more than 1200 East African rift lake species, melanic horizontal stripes have evolved numerous times. We discovered that regulatory changes of the gene agouti-related peptide 2 (agrp2) act as molecular switches controlling this evolutionarily labile phenotype. Reduced agrp2 expression is convergently associated with the presence of stripe patterns across species flocks. However, cis-regulatory mutations are not predictive of stripes across radiations, suggesting independent regulatory mechanisms. Genetic mapping confirms the link between the agrp2 locus and stripe patterns. The crucial role of agrp2 is further supported by a CRISPR-Cas9 knockout that reconstitutes stripes in a nonstriped cichlid. Thus, we unveil how a single gene affects the convergent evolution of a complex color pattern.

Forschungszusammenhang (Projekte)

    Kratochwil, Claudius F.; Sefton, Maggie M.; Liang, Yipeng; Meyer, Axel (2017): Tol2 transposon-mediated transgenesis in the Midas cichlid (Amphilophus citrinellus) : towards understanding gene function and regulatory evolution in an ecological model system for rapid phenotypic diversification BMC Developmental Biology. 2017, 17, 15. eISSN 1471-213X. Available under: doi: 10.1186/s12861-017-0157-x

Tol2 transposon-mediated transgenesis in the Midas cichlid (Amphilophus citrinellus) : towards understanding gene function and regulatory evolution in an ecological model system for rapid phenotypic diversification

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Background
The Midas cichlid species complex (Amphilophus spp.) is widely known among evolutionary biologists as a model system for sympatric speciation and adaptive phenotypic divergence within extremely short periods of time (a few hundred generations). The repeated parallel evolution of adaptive phenotypes in this radiation, combined with their near genetic identity, makes them an excellent model for studying phenotypic diversification. While many ecological and evolutionary studies have been performed on Midas cichlids, the molecular basis of specific phenotypes, particularly adaptations, and their underlying coding and cis-regulatory changes have not yet been studied thoroughly.

Results
For the first time in any New World cichlid, we use Tol2 transposon-mediated transgenesis in the Midas cichlid (Amphilophus citrinellus). By adapting existing microinjection protocols, we established an effective protocol for transgenesis in Midas cichlids. Embryos were injected with a Tol2 plasmid construct that drives enhanced green fluorescent protein (eGFP) expression under the control of the ubiquitin promoter. The transgene was successfully integrated into the germline, driving strong ubiquitous expression of eGFP in the first transgenic Midas cichlid line. Additionally, we show transient expression of two further transgenic constructs, ubiquitin::tdTomato and mitfa::eGFP. Transgenesis in Midas cichlids will facilitate further investigation of the genetic basis of species-specific traits, many of which are adaptations.

Conclusion
Transgenesis is a versatile tool not only for studying regulatory elements such as promoters and enhancers, but also for testing gene function through overexpression of allelic gene variants. As such, it is an important first step in establishing the Midas cichlid as a powerful model for studying adaptive coding and non-coding changes in an ecological and evolutionary context.

Forschungszusammenhang (Projekte)

    Härer, Andreas; Torres-Dowdall, Julián; Meyer, Axel (2017): Rapid adaptation to a novel light environment : The importance of ontogeny and phenotypic plasticity in shaping the visual system of Nicaraguan Midas cichlid fish (Amphilophus citrinellus spp.) Molecular Ecology. 2017, 26(20), pp. 5582-5593. ISSN 0962-1083. eISSN 1365-294X. Available under: doi: 10.1111/mec.14289

Rapid adaptation to a novel light environment : The importance of ontogeny and phenotypic plasticity in shaping the visual system of Nicaraguan Midas cichlid fish (Amphilophus citrinellus spp.)

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Colonization of novel habitats is typically challenging to organisms. In the initial stage after colonization, approximation to fitness optima in the new environment can occur by selection acting on standing genetic variation, modification of developmental patterns or phenotypic plasticity. Midas cichlids have recently colonized crater Lake Apoyo from great Lake Nicaragua. The photic environment of crater Lake Apoyo is shifted towards shorter wavelengths compared to great Lake Nicaragua and Midas cichlids from both lakes differ in visual sensitivity. We investigated the contribution of ontogeny and phenotypic plasticity in shaping the visual system of Midas cichlids after colonizing this novel photic environment. To this end, we measured cone opsin expression both during development and after experimental exposure to different light treatments. Midas cichlids from both lakes undergo ontogenetic changes in cone opsin expression, but visual sensitivity is consistently shifted towards shorter wavelengths in crater lake fish, which leads to a paedomorphic retention of their visual phenotype. This shift might be mediated by lower levels of thyroid hormone in crater lake Midas cichlids (measured indirectly as dio2 and dio3 gene expression). Exposing fish to different light treatments revealed that cone opsin expression is phenotypically plastic in both species during early development, with short and long wavelength light slowing or accelerating ontogenetic changes, respectively. Notably, this plastic response was maintained into adulthood only in the derived crater lake Midas cichlids. We conclude that the rapid evolution of Midas cichlids’ visual system after colonizing crater Lake Apoyo was mediated by a shift in visual sensitivity during ontogeny and was further aided by phenotypic plasticity during development.

Forschungszusammenhang (Projekte)

    Torres-Dowdall, Julián; Golcher-Benavides, Jimena; Machado-Schiaffino, Gonzalo; Meyer, Axel (2017): The role of rare morph advantage and conspicuousness in the stable gold-dark colour polymorphism of a crater lake Midas cichlid fish Journal of Animal Ecology. 2017, 86(5), pp. 1044-1053. ISSN 0021-8790. eISSN 1365-2656. Available under: doi: 10.1111/1365-2656.12693

The role of rare morph advantage and conspicuousness in the stable gold-dark colour polymorphism of a crater lake Midas cichlid fish

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1. Genetically based stable colour polymorphisms provide a unique opportunity to study the evolutionary processes that preserve genetic variability in the wild. Different mechanisms are proposed to promote the stability of polymorphisms, but only few empirical examples have been documented, resulting in an incomplete understanding of these mechanisms.

2. A remarkable genetically determined stable colour polymorphism is found in the Nicaraguan Midas cichlid species complex (Amphilophus cf. citrinellus). All Midas cichlids start their life with a dark-grey coloration (dark morph), but individuals carrying the dominant “gold” allele (c. 10%) lose their melanophores later in life, revealing the underlying orange coloration (gold morph). How this polymorphism is maintained remains unclear. Two main hypotheses have been proposed, both suggesting differential predation upon colour morphs as the proximate mechanism. One predicts that the conspicuous gold morph is more likely to be preyed upon, but this disadvantage is balanced by their competitive dominance over the dark morph. The second hypothesis suggests a rare morph advantage where the rarer gold morph experiences less predation. Empirical evidence for either of these mechanisms is still circumstantial and inconclusive.

3. We conducted two field experiments in a Nicaraguan crater lake using wax models simulating both morphs to determine predation pressure upon Midas cichlid colour morphs. First, we tested the interaction of coloration and depth on attack rate. Second, we tested the interaction of fish size and coloration. We contrasted the pattern of attacks from these experiments to the predicted predation patterns from the hypotheses proposed to explain the colour polymorphism's stability.

4. Large models imitating colour morphs were attacked at similar rates irrespectively of their position in the water column. Yet, attacks upon small models resembling juveniles were directed mainly towards dark models. This resulted in a significant size-by-colour interaction.

5. We suggest that gold Midas cichlids experience a rare morph advantage as juveniles when individuals of this morph are extremely uncommon. But this effect is reduced or disappears among adults, where gold individuals are relatively more common. Thus, the interaction of rare morph advantage and conspicuousness, rather than either of those factors alone, is a likely mechanism resulting in the stability of the colour polymorphism in Midas cichlids.

Forschungszusammenhang (Projekte)

    Henning, Frederico; Machado-Schiaffino, Gonzalo; Baumgarten, Lukas; Meyer, Axel (2017): Genetic dissection of adaptive form and function in rapidly speciating cichlid fishes Evolution. 2017, 71(5), pp. 1297-1312. ISSN 0014-3820. eISSN 1558-5646. Available under: doi: 10.1111/evo.13206

Genetic dissection of adaptive form and function in rapidly speciating cichlid fishes

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Genes of major phenotypic effects and strong genetic correlations can facilitate adaptation, direct selective responses, and potentially lead to phenotypic convergence. However, the preponderance of this type of genetic architecture in repeatedly evolved adaptations remains unknown. Using hybrids between Haplochromis chilotes (thick-lipped) and Pundamilia nyererei (thin-lipped) we investigated the genetics underlying hypertrophied lips and elongated heads, traits that evolved repeatedly in cichlids. At least 25 loci of small-to-moderate and mainly additive effects were detected. Phenotypic variation in lip and head morphology was largely independent. Although several QTL overlapped for lip and head morphology traits, they were often of opposite effects. The distribution of effect signs suggests strong selection on lips. The fitness implications of several detected loci were demonstrated using a laboratory assay testing for the association between genotype and variation in foraging performance. The persistence of low fitness alleles in head morphology appears to be maintained through antagonistic pleiotropy/close linkage with positive-effect lip morphology alleles. Rather than being based on few major loci with strong positive genetic correlations, our results indicate that the evolution of the Lake Victoria thick-lipped ecomorph is the result of selection on numerous loci distributed throughout the genome.

Forschungszusammenhang (Projekte)

    Härer, Andreas; Torres-Dowdall, Julián; Meyer, Axel (2017): The imperiled fish fauna in the Nicaragua Canal zone Conservation Biology. 2017, 31(1), pp. 86-95. ISSN 0888-8892. eISSN 1523-1739. Available under: doi: 10.1111/cobi.12768

The imperiled fish fauna in the Nicaragua Canal zone

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Large-scale infrastructure projects commonly have strong effects on the environment. Thus, it is of highest importance to evaluate possible impacts on biodiversity and take measures to reduce these. The planned construction of the Nicaragua Canal will irreversibly alter the aquatic environment of Nicaragua in many ways. Two distinct drainage basins (San Juan and Punta Gorda) will be connected, fostering biotic homogenization due to establishment of non-native species, extirpation of local species and alteration of numerous ecosystems. Considering the far-reaching impact of this project on Nicaragua's environment, too few studies on biodiversity have been performed in affected areas. This limits the ability to make solid environmental impact assessments. Here, we explore the geographic distribution of taxonomic and genetic diversity from representative freshwater fish species across the Nicaragua Canal Zone. We show that freshwater fish faunas likely differ substantially between drainage basins (Jaccard similarity = 0.33). Further, most populations from distinct drainage basins are highly differentiated based on mitochondrial cytb. Removing the geographic barrier between these basins will promote genetic homogenization and the loss of unique diversity. Moreover, we found species in areas where they were not known to exist and provide insights into the distribution of an undescribed, highly distinct clade of livebearing fish (Poecilia). Our results indicate that the Nicaragua Canal likely will have strong impacts on Nicaragua's freshwater biodiversity. However, knowledge about the extent of these impacts remains scarce, highlighting the need for more thorough investigations to inform more cogently on the status quo before the environment is altered irreversibly.

Forschungszusammenhang (Projekte)

    Franchini, Paolo; Monné Parera, Daniel; Kautt, Andreas F.; Meyer, Axel (2017): quaddRAD : a new high-multiplexing and PCR duplicate removal ddRAD protocol produces novel evolutionary insights in a nonradiating cichlid lineage Molecular Ecology. 2017, 26(10), pp. 2783-2795. ISSN 0962-1083. eISSN 1365-294X. Available under: doi: 10.1111/mec.14077

quaddRAD : a new high-multiplexing and PCR duplicate removal ddRAD protocol produces novel evolutionary insights in a nonradiating cichlid lineage

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The identification of thousands of variants across the genomes and their accurate genotyping are crucial for estimating the genetic parameters needed to address a host of molecular ecological and evolutionary questions. With rapid advances of massively parallel high-throughput sequencing technologies, several methods have recently been developed to access genomewide data on population variation. One of the most successful and widely used techniques relies on the combination of restriction enzymes and sequencing-by-synthesis: restriction-site-associated DNA sequencing (RADSeq). We developed a new, more time- and cost-efficient double-digest RAD paired-end protocol (quaddRAD) that simplifies and speeds up the identification of PCR duplicates and permits large-scale multiplexing. Assessing its performance on a technical data set, we also applied the quaddRAD method on population samples of a Neotropical cichlid fish lineage (Archocentrus centrarchus) to assess its genetic structure and demographic history. While we identified allopatric interlake genetic divergence, most likely driven by drift, no signature of sympatric divergence was detected. This differs from what has been observed in the clade of Midas cichlids (Amphilophus citrinellus spp.), another cichlid lineage that inhabits the same lakes and shares a similar demographic history, but has evolved into small-scale adaptive radiations via sympatric speciation. We demonstrate that quaddRAD is a robust and efficient method for genotyping a massive number and widely overlapping set of loci with high accuracy. Furthermore, the results on A. centrarchus open new research avenues providing an ideal system to investigate genome-level mechanisms that could alter the speciation potential of different but closely related cichlid lineages.

Forschungszusammenhang (Projekte)

    Schneider, Ralf F.; Meyer, Axel (2017): How plasticity, genetic assimilation and cryptic genetic variation may contribute to adaptive radiations Molecular Ecology. 2017, 26(1), pp. 330-350. ISSN 0962-1083. eISSN 1365-294X. Available under: doi: 10.1111/mec.13880

How plasticity, genetic assimilation and cryptic genetic variation may contribute to adaptive radiations

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There is increasing evidence that phenotypic plasticity can promote population divergence by facilitating phenotypic diversification and, eventually, genetic divergence. When a 'plastic' population colonizes a new habitat, it has the possibility to occupy multiple niches by expressing several distinct phenotypes. These initially reflect the population's plastic range but may later become genetically fixed by selection via the process of 'genetic assimilation' (GA). Through this process multiple specialized sister lineages can arise that share a common plastic ancestor - the 'flexible stem'. Here, we review possible molecular mechanisms through which natural selection could fix an initially plastic trait during GA. These mechanisms could also explain how GA may contribute to cryptic genetic variation that can subsequently be coopted into other phenotypes or traits, but also lead to nonadaptive responses. We outline the predicted patterns of genetic and transcriptional divergence accompanying flexible stem radiations. The analysis of such patterns of (retained) adaptive and nonadaptive plastic responses within and across radiating lineages can inform on the state of ongoing GA. We conclude that, depending on the stability of the environment, the molecular architecture underlying plastic traits can facilitate diversification, followed by fixation and consolidation of an adaptive phenotype and degeneration of nonadaptive ones. Additionally, the process of GA may increase the cryptic genetic variation of populations, which on one hand may serve as substrate for evolution, but on another may be responsible for nonadaptive responses that consolidate local allopatry and thus reproductive isolation.

Forschungszusammenhang (Projekte)

    Machado-Schiaffino, Gonzalo; Kautt, Andreas F.; Torres-Dowdall, Julián; Baumgarten, Lukas; Henning, Frederico; Meyer, Axel (2017): Incipient speciation driven by hypertrophied lips in Midas cichlid fishes? Molecular Ecology. 2017, 26(8), pp. 2348-2362. ISSN 0962-1083. eISSN 1365-294X. Available under: doi: 10.1111/mec.14029

Incipient speciation driven by hypertrophied lips in Midas cichlid fishes?

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Sympatric speciation has been debated in evolutionary biology for decades. Although it has gained in acceptance recently, still only a handful of empirical examples are seen as valid (e.g. crater lake cichlids). In this study, we disentangle the role of hypertrophied lips in the repeated adaptive radiations of Nicaraguan crater lake cichlid fish. We assessed the role of disruptive selection and assortative mating during the early stages of divergence and found a functional trade-off in feeding behaviour between thick- and thin-lipped ecotypes, suggesting that this trait is a target of disruptive selection. Thick-lipped fish perform better on nonevasive prey at the cost of a poorer performance on evasive prey. Using enclosures in the wild, we found that thick-lipped fish perform significantly better in rocky than in sandy habitats. We found almost no mixed pairs during two breeding seasons and hence significant assortative mating. Genetic differentiation between ecotypes seems to be related to the time since colonization, being subtle in L. Masaya (1600 generations ago) and absent in the younger L. Apoyeque (<600 generations ago). Genome-wide differentiation between ecotypes was higher in the old source lakes than in the young crater lakes. Our results suggest that hypertrophied lips might be promoting incipient sympatric speciation through divergent selection (ecological divergence in feeding performance) and nonrandom mating (assortative mating) in the young Nicaraguan crater lakes. Nonetheless, further manipulative experiments are needed in order to confirm the role of hypertrophied lips as the main cue for assortative mating.

Forschungszusammenhang (Projekte)

    Torres-Dowdall, Julián; Pierotti, Michele E. R.; Härer, Andreas; Karagic, Nidal; Woltering, Joost M.; Henning, Frederico; Elmer, Kathryn R.; Meyer, Axel (2017): Rapid and Parallel Adaptive Evolution of the Visual System of Neotropical Midas Cichlid Fishes Molecular biology and evolution. 2017, 34(10), pp. 2469-2485. ISSN 0737-4038. eISSN 1537-1719. Available under: doi: 10.1093/molbev/msx143

Rapid and Parallel Adaptive Evolution of the Visual System of Neotropical Midas Cichlid Fishes

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Midas cichlid fish are a Central American species flock containing 13 described species that has been dated to only a few thousand years old, a historical timescale infrequently associated with speciation. Their radiation involved the colonization of several clear water crater lakes from two turbid great lakes. Therefore, Midas cichlids have been subjected to widely varying photic conditions during their radiation. Being a primary signal relay for information from the environment to the organism, the visual system is under continuing selective pressure and a prime organ system for accumulating adaptive changes during speciation, particularly in the case of dramatic shifts in photic conditions. Here, we characterize the full visual system of Midas cichlids at organismal and genetic levels, to determine what types of adaptive changes evolved within the short time span of their radiation. We show that Midas cichlids have a diverse visual system with unexpectedly high intra- and interspecific variation in color vision sensitivity and lens transmittance. Midas cichlid populations in the clear crater lakes have convergently evolved visual sensitivities shifted toward shorter wavelengths compared with the ancestral populations from the turbid great lakes. This divergence in sensitivity is driven by changes in chromophore usage, differential opsin expression, opsin coexpression, and to a lesser degree by opsin coding sequence variation. The visual system of Midas cichlids has the evolutionary capacity to rapidly integrate multiple adaptations to changing light environments. Our data may indicate that, in early stages of divergence, changes in opsin regulation could precede changes in opsin coding sequence evolution.

Forschungszusammenhang (Projekte)

    Fruciano, Carmelo; Franchini, Paolo; Kovacova, Viera; Elmer, Kathryn R.; Henning, Frederico; Meyer, Axel (2016): Genetic linkage of distinct adaptive traits in sympatrically speciating crater lake cichlid fish Nature Communications. 2016, 7, 12736. eISSN 2041-1723. Available under: doi: 10.1038/ncomms12736

Genetic linkage of distinct adaptive traits in sympatrically speciating crater lake cichlid fish

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Our understanding of how biological diversity arises is limited, especially in the case of speciation in the face of gene flow. Here we investigate the genomic basis of adaptive traits, focusing on a sympatrically diverging species pair of crater lake cichlid fishes. We identify the main quantitative trait loci (QTL) for two eco-morphological traits: body shape and pharyngeal jaw morphology. These traits diverge in parallel between benthic and limnetic species in the repeated adaptive radiations of this and other fish lineages. Remarkably, a single chromosomal region contains the highest effect size QTL for both traits. Transcriptomic data show that the QTL regions contain genes putatively under selection. Independent population genomic data corroborate QTL regions as areas of high differentiation between the sympatric sister species. Our results provide empirical support for current theoretical models that emphasize the importance of genetic linkage and pleiotropy in facilitating rapid divergence in sympatry.

Forschungszusammenhang (Projekte)

    Kautt, Andreas F.; Machado-Schiaffino, Gonzalo; Torres-Dowdall, Julián; Meyer, Axel (2016): Incipient sympatric speciation in Midas cichlid fish from the youngest and one of the smallest crater lakes in Nicaragua due to differential use of the benthic and limnetic habitats? Ecology and Evolution. 2016, 6(15), pp. 5342-5357. eISSN 2045-7758. Available under: doi: 10.1002/ece3.2287

Incipient sympatric speciation in Midas cichlid fish from the youngest and one of the smallest crater lakes in Nicaragua due to differential use of the benthic and limnetic habitats?

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Understanding how speciation can occur without geographic isolation remains a central objective in evolutionary biology. Generally, some form of disruptive selection and assortative mating are necessary for sympatric speciation to occur. Disruptive selection can arise from intraspecific competition for resources. If this competition leads to the differential use of habitats and variation in relevant traits is genetically determined, then assortative mating can be an automatic consequence (i.e., habitat isolation). In this study, we caught Midas cichlid fish from the limnetic (middle of the lake) and benthic (shore) habitats of Crater Lake Asososca Managua to test whether some of the necessary conditions for sympatric speciation due to intraspecific competition and habitat isolation are given. Lake As. Managua is very small (<900 m in diameter), extremely young (maximally 1245 years of age), and completely isolated. It is inhabited by, probably, only a single endemic species of Midas cichlids, Amphilophus tolteca. We found that fish from the limnetic habitat were more elongated than fish collected from the benthic habitat, as would be predicted from ecomorphological considerations. Stable isotope analyses confirmed that the former also exhibit a more limnetic lifestyle than the latter. Furthermore, split-brood design experiments in the laboratory suggest that phenotypic plasticity is unlikely to explain much of the observed differences in body elongation that we observed in the field. Yet, neutral markers (microsatellites) did not reveal any genetic clustering in the population. Interestingly, demographic inferences based on RAD-seq data suggest that the apparent lack of genetic differentiation at neutral markers could simply be due to a lack of time, as intraspecific competition may only have begun a few hundred generations ago.

Forschungszusammenhang (Projekte)

    Kautt, Andreas F.; Machado-Schiaffino, Gonzalo; Meyer, Axel (2016): Multispecies Outcomes of Sympatric Speciation after Admixture with the Source Population in Two Radiations of Nicaraguan Crater Lake Cichlids PLoS Genetics. 2016, 12(6), e1006157. ISSN 1553-7390. eISSN 1553-7404. Available under: doi: 10.1371/journal.pgen.1006157

Multispecies Outcomes of Sympatric Speciation after Admixture with the Source Population in Two Radiations of Nicaraguan Crater Lake Cichlids

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The formation of species in the absence of geographic barriers (i.e. sympatric speciation) remains one of the most controversial topics in evolutionary biology. While theoretical models have shown that this most extreme case of primary divergence-with-gene-flow is possible, only a handful of accepted empirical examples exist. And even for the most convincing examples uncertainties remain; complex histories of isolation and secondary contact can make species falsely appear to have originated by sympatric speciation. This alternative scenario is notoriously difficult to rule out. Midas cichlids inhabiting small and remote crater lakes in Nicaragua are traditionally considered to be one of the best examples of sympatric speciation and lend themselves to test the different evolutionary scenarios that could lead to apparent sympatric speciation since the system is relatively small and the source populations known. Here we reconstruct the evolutionary history of two small-scale radiations of Midas cichlids inhabiting crater lakes Apoyo and Xiloá through a comprehensive genomic data set. We find no signs of differential admixture of any of the sympatric species in the respective radiations. Together with coalescent simulations of different demographic models our results support a scenario of speciation that was initiated in sympatry and does not result from secondary contact of already partly diverged populations. Furthermore, several species seem to have diverged simultaneously, making Midas cichlids an empirical example of multispecies outcomes of sympatric speciation. Importantly, however, the demographic models strongly support an admixture event from the source population into both crater lakes shortly before the onset of the radiations within the lakes. This opens the possibility that the formation of reproductive barriers involved in sympatric speciation was facilitated by genetic variants that evolved in a period of isolation between the initial founding population and the secondary migrants that came from the same source population. Thus, the exact mechanisms by which these species arose might be different from what had been thought before.

Forschungszusammenhang (Projekte)

    Franchini, Paolo; Xiong, Peiwen; Fruciano, Carmelo; Meyer, Axel (2016): The Role of microRNAs in the Repeated Parallel Diversification of Lineages of Midas Cichlid Fish from Nicaragua Genome Biology and Evolution. 2016, 8(5), pp. 1543-1555. eISSN 1759-6653. Available under: doi: 10.1093/gbe/evw097

The Role of microRNAs in the Repeated Parallel Diversification of Lineages of Midas Cichlid Fish from Nicaragua

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Cichlid fishes are an ideal model system for studying biological diversification because they provide textbook examples of rapid speciation. To date, there has been little focus on the role of gene regulation during cichlid speciation. However, in recent years, gene regulation has been recognized as a powerful force linking diversification in gene function to speciation. Here, we investigated the potential role of miRNA regulation in the diversification of six cichlid species of the Midas cichlid lineage (Amphilophus spp.) inhabiting the Nicaraguan crater lakes. Using several genomic resources, we inferred 236 Midas miRNA genes that were used to predict the miRNA target sites on 8,232 Midas 3'-UTRs. Using population genomic calculations of SNP diversity, we found the miRNA genes to be more conserved than protein coding genes. In contrast to what has been observed in other cichlid fish, but similar to what has been typically found in other groups, we observed genomic signatures of purifying selection on the miRNA targets by comparing these sites with the less conserved nontarget portion of the 3'-UTRs. However, in one species pair that has putatively speciated sympatrically in crater Lake Apoyo, we recovered a different pattern of relaxed purifying selection and high genetic divergence at miRNA targets. Our results suggest that sequence evolution at miRNA binding sites could be a critical genomic mechanism contributing to the rapid phenotypic evolution of Midas cichlids.

Forschungszusammenhang (Projekte)

    Fruciano, Carmelo; Franchini, Paolo; Raffini, Francesca; Fan, Shaohua; Meyer, Axel (2016): Are sympatrically speciating Midas cichlid fish special? : Patterns of morphological and genetic variation in the closely related species Archocentrus centrarchus Ecology and Evolution. 2016, 6(12), pp. 4102-4114. eISSN 2045-7758. Available under: doi: 10.1002/ece3.2184

Are sympatrically speciating Midas cichlid fish special? : Patterns of morphological and genetic variation in the closely related species Archocentrus centrarchus

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Established empirical cases of sympatric speciation are scarce, although there is an increasing consensus that sympatric speciation might be more common than previously thought. Midas cichlid fish are one of the few substantiated cases of sympatric speciation, and they formed repeated radiations in crater lakes. In contrast, in the same environment, such radiation patterns have not been observed in other species of cichlids and other families of fish. We analyze morphological and genetic variation in a cichlid species (Archocentrus centrarchus) that co-inhabits several crater lakes with the Midas species complex. In particular, we analyze variation in body and pharyngeal jaw shape (two ecologically important traits in sympatrically divergent Midas cichlids) and relate that to genetic variation in mitochondrial control region and microsatellites. Using these four datasets, we analyze variation between and within two Nicaraguan lakes: a crater lake where multiple Midas cichlids have been described and a lake where the source population lives. We do not observe any within-lake clustering consistent across morphological traits and genetic markers, suggesting the absence of sympatric divergence in A. centrarchus. Genetic differentiation between lakes was low and morphological divergence absent. Such morphological similarity between lakes is found not only in average morphology, but also when analyzing covariation between traits and degree of morphospace occupation. A combined analysis of the mitochondrial control region in A. centrarchus and Midas cichlids suggests that a difference between lineages in the timing of crater lake colonization cannot be invoked as an explanation for the difference in their levels of diversification. In light of our results, A. centrarchus represents the ideal candidate to study the genomic differences between these two lineages that might explain why some lineages are more likely to speciate and diverge in sympatry than others.

Forschungszusammenhang (Projekte)

    Torres-Dowdall, Julián; Henning, Frederico; Elmer, Kathryn R.; Meyer, Axel (2015): Ecological and Lineage-Specific Factors Drive the Molecular Evolution of Rhodopsin in Cichlid Fishes Molecular Biology and Evolution. 2015, 32(11), pp. 2876-2882. ISSN 0737-4038. eISSN 1537-1719. Available under: doi: 10.1093/molbev/msv159

Ecological and Lineage-Specific Factors Drive the Molecular Evolution of Rhodopsin in Cichlid Fishes

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The visual system in the colorful cichlid fishes from the African great lakes is believed to be important for their adaptive radiations. However, few studies have attempted to compare the visual system of radiating cichlid lineages with that of cichlids that have not undergone recent radiations. One such study published in this journal (Schott RK, Refvik SP, Hauser FE, López-Fernández H, Chang BSW. 2014. Divergent positive selection in rhodopsin from lake and riverine cichlid fishes. Mol Biol Evol. 31:1149–1165) found divergent selection on rhodopsin between African lacustrine and riverine cichlid species and riverine Neotropical cichlids, concluding that ecology drives the molecular evolution of this opsin. Here, we expand this analysis by incorporating rhodopsin sequences from Neotropical lacustrine cichlids and show that both ecology and phylogeny are important drivers of the molecular evolution of rhodopsin in cichlids. We found little overlap of sites under selection between African and Neotropical lineages and a faster rate of molecular evolution in African compared with Neotropical cichlids. These results support the notion that genetic or population genetic features particular to African cichlids contributed to their radiations.

Forschungszusammenhang (Projekte)

    Kratochwil, Claudius F.; Meyer, Axel (2015): Closing the genotype-phenotype gap : Emerging technologies for evolutionary genetics in ecological model vertebrate systems BioEssays. 2015, 37(2), pp. 213-226. ISSN 0265-9247. eISSN 1521-1878. Available under: doi: 10.1002/bies.201400142

Closing the genotype-phenotype gap : Emerging technologies for evolutionary genetics in ecological model vertebrate systems

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The analysis of genetic and epigenetic mechanisms of the genotype–phenotypic connection has, so far, only been possible in a handful of genetic model systems. Recent technological advances, including next-generation sequencing methods such as RNA-seq, ChIP-seq and RAD-seq, and genome-editing approaches including CRISPR-Cas, now permit to address these fundamental questions of biology also in organisms that have been studied in their natural habitats. We provide an overview of the benefits and drawbacks of these novel techniques and experimental approaches that can now be applied to ecological and evolutionary vertebrate models such as sticklebacks and cichlid fish. We can anticipate that these new methods will increase the understanding of the genetic and epigenetic factors influencing adaptations and phenotypic variation in ecological settings. These new arrows in the methodological quiver of ecologist will drastically increase the understanding of the genetic basis of adaptive traits – leading to a further closing of the genotype–phenotype gap.

Forschungszusammenhang (Projekte)

    Machado-Schiaffino, Gonzalo; Kautt, Andreas F.; Kusche, Henrik; Meyer, Axel (2015): Parallel evolution in Ugandan crater lakes : repeated evolution of limnetic body shapes in haplochromine cichlid fish BMC Evolutionary Biology. 2015, 15, 9. eISSN 1471-2148. Available under: doi: 10.1186/s12862-015-0287-3

Parallel evolution in Ugandan crater lakes : repeated evolution of limnetic body shapes in haplochromine cichlid fish

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Background
The enormous diversity found in East African cichlid fishes in terms of morphology, coloration, and behavior have made them a model for the study of speciation and adaptive evolution. In particular, haplochromine cichlids, by far the most species-rich lineage of cichlids, are a well-known textbook example for parallel evolution. Southwestern Uganda is an area of high tectonic activity, and is home to numerous crater lakes. Many Ugandan crater lakes were colonized, apparently independently, by a single lineage of haplochromine cichlids. Thereby, this system could be considered a natural experiment in which one can study the interaction between geographical isolation and natural selection promoting phenotypic diversification.

Results
We sampled 13 crater lakes and six potentially-ancestral older lakes and, using both mitochondrial and microsatellite markers, discovered strong genetic and morphological differentiation whereby (a) geographically close lakes tend to be genetically more similar and (b) three different geographic areas seem to have been colonized by three independent waves of colonization from the same source population. Using a geometric morphometric approach, we found that body shape elongation (i.e. a limnetic morphology) evolved repeatedly from the ancestral deeper-bodied benthic morphology in the clear and deep crater lake habitats.

Conclusions
A pattern of strong genetic and morphological differentiation was observed in the Ugandan crater lakes. Our data suggest that body shape changes have repeatedly evolved into a more limnetic-like form in several Ugandan crater lakes after independent waves of colonization from the same source population. The observed morphological changes in crater lake cichlids are likely to result from a common selective regime.

Forschungszusammenhang (Projekte)

    Kratochwil, Claudius F.; Geißler, Laura; Irisarri, Iker; Meyer, Axel (2015): Molecular Evolution of the Neural Crest Regulatory Network in Ray-Finned Fish Genome Biology and Evolution. 2015, 7(11), pp. 3033-3046. eISSN 1759-6653. Available under: doi: 10.1093/gbe/evv200

Molecular Evolution of the Neural Crest Regulatory Network in Ray-Finned Fish

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Gene regulatory networks (GRN) are central to developmental processes. They are composed of transcription factors and signaling molecules orchestrating gene expression modules that tightly regulate the development of organisms. The neural crest (NC) is a multipotent cell population that is considered a key innovation of vertebrates. Its derivatives contribute to shaping the astounding morphological diversity of jaws, teeth, head skeleton, or pigmentation. Here, we study the molecular evolution of the NC GRN by analyzing patterns of molecular divergence for a total of 36 genes in 16 species of bony fishes. Analyses of nonsynonymous to synonymous substitution rate ratios (dN/dS) support patterns of variable selective pressures among genes deployed at different stages of NC development, consistent with the developmental hourglass model. Model-based clustering techniques of sequence features support the notion of extreme conservation of NC-genes across the entire network. Our data show that most genes are under strong purifying selection that is maintained throughout ray-finned fish evolution. Late NC development genes reveal a pattern of increased constraints in more recent lineages. Additionally, seven of the NC-genes showed signs of relaxation of purifying selection in the famously species-rich lineage of cichlid fishes. This suggests that NC genes might have played a role in the adaptive radiation of cichlids by granting flexibility in the development of NC-derived traits-suggesting an important role for NC network architecture during the diversification in vertebrates.

Forschungszusammenhang (Projekte)

    Kusche, Henrik; Elmer, Kathryn R.; Meyer, Axel (2015): Sympatric ecological divergence associated with a color polymorphism BMC Biology. 2015, 13, 82. eISSN 1741-7007. Available under: doi: 10.1186/s12915-015-0192-7

Sympatric ecological divergence associated with a color polymorphism

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Background
Color polymorphisms are a conspicuous feature of many species and a way to address broad ecological and evolutionary questions. Three potential major evolutionary fates of color polymorphisms are conceivable over time: maintenance, loss, or speciation. However, the understanding of color polymorphisms and their evolutionary implications is frequently impaired by sex-linkage of coloration, unknown inheritance patterns, difficulties in phenotypic characterization, and a lack of evolutionary replicates. Hence, the role of color polymorphisms in promoting ecological and evolutionary diversification remains poorly understood. In this context, we assessed the ecological and evolutionary consequences of a color polymorphic study system that is not hampered by these restrictions: the repeated adaptive radiations of the gold/dark Midas cichlid fishes (the Amphilophus citrinellus species complex) from the great lakes and crater lakes of Nicaragua, Central America.

Results
We conducted multi-trait morphological and ecological analyses from ten populations of this young adaptive radiation (<6,000 years old), which revealed sympatric ecological differentiation associated with the conspicuous binary (gold/dark) color polymorphism. Varying degrees of intraspecific ecological divergence were observed across the ten color morph pairs, but most pairs exhibited a consistently parallel ecological and evolutionary trajectory across populations. Specifically, gold Midas cichlids are frequently deeper-bodied, have more robust pharyngeal jaws, and feed at a lower trophic level compared to conspecific, sympatric dark individuals. A common garden experiment suggests there is a genetic correlation of color and eco-morphological traits.

Conclusions
We demonstrate unprecedented ecological and evolutionary consequences of color polymorphism in this adaptive radiation. Across the species complex, sympatric conspecific individuals differed in eco-morphology depending on color morph (gold/dark) and the axis of differentiation tended to be consistent across replicates. The consistent divergence across wild populations and the common garden experiment suggests that color is genetically correlated to ecology. Because Midas cichlids are known to mate color assortatively, the putative genetic correlation of this color polymorphism with an eco-morphological divergence suggests an innate potential to promote ecological and evolutionary divergence across this species complex. However, there are to date no examples of speciation based on color in this radiation, suggesting long-term maintenance of this color polymorphism.

Forschungszusammenhang (Projekte)

    Kratochwil, Claudius F.; Sefton, Maggie M.; Meyer, Axel (2015): Embryonic and larval development in the Midas cichlid fish species flock (Amphilophus spp.) : a new evo-devo model for the investigation of adaptive novelties and species differences BMC Developmental Biology. 2015, 15, 12. eISSN 1471-213X. Available under: doi: 10.1186/s12861-015-0061-1

Embryonic and larval development in the Midas cichlid fish species flock (Amphilophus spp.) : a new evo-devo model for the investigation of adaptive novelties and species differences

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Background

Central American crater lake cichlid fish of the Midas species complex (Amphilophus spp.) are a model system for sympatric speciation and fast ecological diversification and specialization. Midas cichlids have been intensively analyzed from an ecological and morphological perspective. Genomic resources such as transcriptomic and genomic data sets, and a high-quality draft genome are available now. Many ecologically relevant species-specific traits and differences such as pigmentation and cranial morphology arise during development. Detailed descriptions of the early development of the Midas cichlid in particular, will help to investigate the ontogeny of species differences and adaptations.

Results

We describe the embryonic and larval development of the crater lake cichlid, Amphilophus xiloaensis, until seven days after fertilization. Similar to previous studies on teleost development, we describe six periods of embryogenesis - the zygote, cleavage, blastula, gastrula, segmentation, and post-hatching period. Furthermore, we define homologous stages to well-described teleost models such as medaka and zebrafish, as well as other cichlid species such as the Nile tilapia and the South American cichlid Cichlasoma dimerus. Key morphological differences between the embryos of Midas cichlids and other teleosts are highlighted and discussed, including the presence of adhesive glands and different early chromatophore patterns, as well as variation in developmental timing.

Conclusions

The developmental staging of the Midas cichlid will aid researchers in the comparative investigation of teleost ontogenies. It will facilitate comparative developmental biological studies of Neotropical and African cichlid fish in particular. In the past, the species flocks of the African Great Lakes have received the most attention from researchers, but some lineages of the 300–400 species of Central American lakes are fascinating model systems for adaptive radiation and rapid phenotypic evolution. The availability of genetic resources, their status as a model system for evolutionary research, and the possibility to perform functional experiments including transgenesis makes the Midas cichlid complex a very attractive model for evolutionary-developmental research.

Forschungszusammenhang (Projekte)

    Baumgarten, Lukas; Machado-Schiaffino, Gonzalo; Henning, Frederico; Meyer, Axel (2015): What big lips are good for : on the adaptive function of repeatedly evolved hypertrophied lips of cichlid fishes Biological Journal of the Linnean Society. 2015, 115(2), pp. 448-455. ISSN 0024-4066. eISSN 1095-8312. Available under: doi: 10.1111/bij.12502

What big lips are good for : on the adaptive function of repeatedly evolved hypertrophied lips of cichlid fishes

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Linking phenotypic traits to an adaptive ecological function is a major goal of evolutionary biology. However, this task is challenging and has been accomplished in only a handful of species and ecological model systems. The repeatedly evolved adaptive radiations of cichlid fishes are composed of an enormously diverse set of species that differ in trophic morphology, body shape, coloration, and behaviour. Ecological guilds of species with conspicuously hypertrophied lips have evolved in parallel in all major cichlid radiations and are characterized by large lips and pointed and narrow heads. In the present study, we experimentally tested the adaptive significance of this set of conspicuous traits by comparing the success of hypertrophied-lipped and closely-related thin-lipped endemic Lake Victoria cichlids in a novel foraging assay. The hypertrophied-lipped species (Haplochromis chilotes) was clearly more successful in exploiting food resources from narrow crevices and the observed difference in foraging success increased more at narrower angles. Furthermore, pronounced differences in exploratory behaviour between the species suggest that the evolution of hypertrophied-lipped species involved the co-evolution of a suite of traits that include foraging behaviour. The repeated evolution of hypertrophied-lip morphology in conjunction with a narrow and pointed head shape in cichlids represents an evolutionary innovation that facilitates foraging in rocky crevices, thus allowing access to a novel niche

Forschungszusammenhang (Projekte)

    Machado-Schiaffino, Gonzalo; Henning, Frederico; Meyer, Axel (2014): Species-specific differences in adaptive phenotypic plasticity in an ecologically relevant trophic trait : hypertrophic lips in midas cichlid fishes Evolution. 2014, 68(7), pp. 2086-2091. ISSN 0014-3820. eISSN 1558-5646. Available under: doi: 10.1111/evo.12367

Species-specific differences in adaptive phenotypic plasticity in an ecologically relevant trophic trait : hypertrophic lips in midas cichlid fishes

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The spectacular species richness of cichlids and their diversity in morphology, coloration, and behavior have made them an ideal model for the study of speciation and adaptive evolution. Hypertrophic lips evolved repeatedly and independently in African and Neotropical cichlid radiations. Cichlids with hypertrophic lips forage predominantly in rocky crevices and it has been hypothesized that mechanical stress caused by friction could result in larger lips through phenotypic plasticity. To test the influence of the environment on the size and development of lips, we conducted a series of breeding and feeding experiments on Midas cichlids. Full-sibs of Amphilophus labiatus (thick-lipped) and Amphilophus citrinellus (thin-lipped) each were split into a control group which was fed food from the water column and a treatment group whose food was fixed to substrates. We found strong evidence for phenotypic plasticity on lip area in the thick-lipped species, but not in the thin-lipped species. Intermediate phenotypic values were observed in hybrids from thick- and thin-lipped species reared under “control” conditions. Thus, both a genetic, but also a phenotypic plastic component is involved in the development of hypertrophic lips in Neotropical cichlids. Moreover, species-specific adaptive phenotypic plasticity was found, suggesting that plasticity is selected for in recent thick-lipped species.

Forschungszusammenhang (Projekte)

    Recknagel, Hans; Elmer, Kathryn R.; Meyer, Axel (2014): Crater lake habitat predicts morphological diversity in adaptive radiations of cichlid fishes Evolution. 2014, 68(7), pp. 2145-2155. ISSN 0014-3820. eISSN 1558-5646. Available under: doi: 10.1111/evo.12412

Crater lake habitat predicts morphological diversity in adaptive radiations of cichlid fishes

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Adaptive radiations provide an excellent opportunity for studying the correlates and causes for the origin of biodiversity. In these radiations, species diversity may be influenced by either the ecological and physical environment, intrinsic lineage effects, or both. Disentangling the relative contributions of these factors in generating biodiversity remains a major challenge in understanding why a lineage does or does not radiate. Here, we examined morphological variation in body shape for replicate flocks of Nicaraguan Midas cichlid fishes and tested its association with biological and physical characteristics of their crater lakes. We found that variability of body elongation, an adaptive trait in freshwater fishes, is mainly predicted by average lake depth (N = 6, P < 0.001, R2 = 0.96). Other factors considered, including lake age, surface area, littoral zone area, number of co-occurring fish species, and genetic diversity of the Midas flock, did not significantly predict morphological variability. We also showed that lakes with a larger littoral zone have on average higher bodied Midas cichlids, indicating that Midas cichlid flocks are locally adapted to their crater lake habitats. In conclusion, we found that a lake's habitat predicts the magnitude and the diversity of body elongation in repeated cichlid adaptive radiations.

Forschungszusammenhang (Projekte)

    Franchini, Paolo; Fruciano, Carmelo; Spreitzer, Maria L.; Jones, Julia; Elmer, Kathryn R.; Henning, Frederico; Meyer, Axel (2014): Genomic architecture of ecologically divergent body shape in a pair of sympatric crater lake cichlid fishes Molecular Ecology. 2014, 23(7), pp. 1828-1845. ISSN 0962-1083. eISSN 1365-294X. Available under: doi: 10.1111/mec.12590

Genomic architecture of ecologically divergent body shape in a pair of sympatric crater lake cichlid fishes

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Determining the genetic bases of adaptations and their roles in speciation is a prominent issue in evolutionary biology. Cichlid fish species flocks are a prime example of recent rapid radiations, often associated with adaptive phenotypic divergence from a common ancestor within a short period of time. In several radiations of freshwater fishes, divergence in ecomorphological traits — including body shape, colour, lips and jaws — is thought to underlie their ecological differentiation, specialization and, ultimately, speciation. The Midas cichlid species complex (Amphilophus spp.) of Nicaragua provides one of the few known examples of sympatric speciation where species have rapidly evolved different but parallel morphologies in young crater lakes. This study identified significant QTL for body shape using SNPs generated via ddRAD sequencing and geometric morphometric analyses of a cross between two ecologically and morphologically divergent, sympatric cichlid species endemic to crater Lake Apoyo: an elongated limnetic species (Amphilophus zaliosus) and a high-bodied benthic species (Amphilophus astorquii). A total of 453 genome-wide informative SNPs were identified in 240 F2 hybrids. These markers were used to construct a genetic map in which 25 linkage groups were resolved. Seventy-two segregating SNPs were linked to 11 QTL. By annotating the two most highly supported QTL-linked genomic regions, genes that might contribute to divergence in body shape along the benthic–limnetic axis in Midas cichlid sympatric adaptive radiations were identified. These results suggest that few genomic regions of large effect contribute to early stage divergence in Midas cichlids.

Forschungszusammenhang (Projekte)

    Kusche, Henrik; Recknagel, Hans; Elmer, Kathryn R.; Meyer, Axel (2014): Crater lake cichlids individually specialize along the benthic-limnetic axis Ecology and Evolution. 2014, 4(7), pp. 1127-1139. ISSN 2045-7758. eISSN 2045-7758. Available under: doi: 10.1002/ece3.1015

Crater lake cichlids individually specialize along the benthic-limnetic axis

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A common pattern of adaptive diversification in freshwater fishes is the repeated evolution of elongated open water (limnetic) species and high-bodied shore (benthic) species from generalist ancestors. Studies on phenotype-diet correlations have suggested that population-wide individual specialization occurs at an early evolutionary and ecological stage of divergence and niche partitioning. This variable restricted niche use across individuals can provide the raw material for earliest stages of sympatric divergence. We investigated variation in morphology and diet as well as their correlations along the benthic-limnetic axis in an extremely young Midas cichlid species, Amphilophus tolteca, endemic to the Nicaraguan crater lake Asososca Managua. We found that A. tolteca varied continuously in ecologically relevant traits such as body shape and lower pharyngeal jaw morphology. The correlation of these phenotypes with niche suggested that individuals are specialized along the benthic-limnetic axis. No genetic differentiation within the crater lake was detected based on genotypes from 13 microsatellite loci. Overall, we found that individual specialization in this young crater lake species encompasses the limnetic- as well as the benthic macro-habitat. Yet there is no evidence for any diversification within the species, making this a candidate system for studying what might be the early stages preceding sympatric divergence.

Forschungszusammenhang (Projekte)

    Kusche, Henrik; Meyer, Axel (2014): One cost of being gold : selective predation and implications for the maintenance of the Midas cichlid colour polymorphism (Perciformes: Cichlidae) Biological Journal of the Linnean Society. 2014, 111(2), pp. 350-358. ISSN 0024-4066. eISSN 1095-8312. Available under: doi: 10.1111/bij.12205

One cost of being gold : selective predation and implications for the maintenance of the Midas cichlid colour polymorphism (Perciformes: Cichlidae)

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In the colour-polymorphic Midas cichlid fish species complex (Amphilophus citrinellus spp.), gold morphs occur at much lower frequencies (< 10%) than dark individuals. This might be surprising because gold coloration is dominant and coded for by a single Mendelian locus. Furthermore, gold individuals are considered to be competitively advantaged over dark ones because they grow faster and win aggressive encounters more often compared to dark individuals of equal size. However, one might expect a cost of being gold in terms of natural selection as a result of predation. We tested whether the Jaguar cichlid (Parachromis managuensis), a major fish predator of Midas cichlids, preys differentially on colour variants of goldfish (Carassius auratus auratus), which were used as a proxy for Midas cichlids because of their similarity in colour. Size-matched pairs of prey fish (gold and dark) were offered to the predator and the time until the fish were attacked was recorded. The gold morph was attacked first more often (approximately 70%) but not faster than the dark morph. This suggests that the predator perceives the gold individual first, and/or that the predator exhibits a preference or higher motivation to attack the gold prey fish. The increased risk of predation of gold prey fish suggests for the Midas cichlid system that being gold may carry significant costs in terms of natural selection as a result of its major piscivorous predator.

Forschungszusammenhang (Projekte)

    Torres-Dowdall, Julián; Machado-Schiaffino, Gonzalo; Kautt, Andreas F.; Kusche, Henrik; Meyer, Axel (2014): Differential predation on the two colour morphs of Nicaraguan Crater lake Midas cichlid fish : implications for the maintenance of its gold-dark polymorphism Biological Journal of the Linnean Society. 2014, 112(1), pp. 123-131. ISSN 0024-4066. eISSN 1095-8312. Available under: doi: 10.1111/bij.12271

Differential predation on the two colour morphs of Nicaraguan Crater lake Midas cichlid fish : implications for the maintenance of its gold-dark polymorphism

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Predation can play an important role in the evolution and maintenance of prey colour polymorphisms. Several factors are known to affect predator choice, including the prey's relative abundance and conspicuousness. In polymorphic prey species, predators often target the most common or most visible morphs. To test if predator choice can explain why in Midas cichlid fish the more visible (gold) morph is also more rare than the inconspicuous dark morph, we conducted predation experiments using two differently coloured wax models in Nicaraguan crater lakes. Contrary to expectations, we observed an overall higher attack rate on the much more abundant, yet less conspicuous dark models, and propose frequency-dependent predation as a potential explanation for this result. Interestingly, the attack rate differed between different types of predators. While avian predators were biased towards the abundant and less colourful dark morphs, fish predators did not show a strong bias. However, the relative attack rate of fish predators seemed to vary with the clarity of the water, as attack rates on gold models went up as water clarity decreased. The relative differential predation rates on different morphs might impact the relative abundance of both colour morphs and thus explain the maintenance of the colour polymorphism.

Forschungszusammenhang (Projekte)

    Elmer, Kathryn R.; Fan, Shaohua; Kusche, Henrik; Spreitzer, Maria Luise; Kautt, Andreas F.; Franchini, Paolo; Meyer, Axel (2014): Parallel evolution of Nicaraguan crater lake cichlid fishes via non-parallel routes Nature Communications. 2014, 5, 5168. eISSN 2041-1723. Available under: doi: 10.1038/ncomms6168

Parallel evolution of Nicaraguan crater lake cichlid fishes via non-parallel routes

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Fundamental to understanding how biodiversity arises and adapts is whether evolution is predictable in the face of stochastic genetic and demographic factors. Here we show rapid parallel evolution across two closely related but geographically isolated radiations of Nicaraguan crater lake cichlid fishes. We find significant morphological, ecological and genetic differentiation between ecomorphs in sympatry, reflected primarily in elongated versus high-bodied shape, differential ecological niche use and genetic differentiation. These eco-morphological divergences are significantly parallel across radiations. Based on 442,644 genome-wide single nucleotide polymorphisms, we identify strong support for the monophyly of, and subsequent sympatric divergence within, each radiation. However, the order of speciation differs across radiations; in one lake the limnetic ecomorph diverged first while in the other a benthic ecomorph. Overall our results demonstrate that complex parallel phenotypes can evolve very rapidly and repeatedly in similar environments, probably due to natural selection, yet this evolution can proceed along different evolutionary genetic routes.

Forschungszusammenhang (Projekte)

    Manousaki, Tereza; Hull, Pincelli M.; Kusche, Henrik; Machado-Schiaffino, Gonzalo; Franchini, Paolo; Harrod, Chris; Elmer, Kathryn R.; Meyer, Axel (2013): Parsing parallel evolution : ecological divergence and differential gene expression in the adaptive radiations of thick-lipped Midas cichlid fishes from Nicaragua Molecular Ecology. 2013, 22(3), pp. 650-669. ISSN 0962-1083. eISSN 1365-294X. Available under: doi: 10.1111/mec.12034

Parsing parallel evolution : ecological divergence and differential gene expression in the adaptive radiations of thick-lipped Midas cichlid fishes from Nicaragua

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The study of parallel evolution facilitates the discovery of common rules of diversification. Here, we examine the repeated evolution of thick lips in Midas cichlid fishes (the Amphilophus citrinellus species complex)-from two Great Lakes and two crater lakes in Nicaragua-to assess whether similar changes in ecology, phenotypic trophic traits and gene expression accompany parallel trait evolution. Using next-generation sequencing technology, we characterize transcriptome-wide differential gene expression in the lips of wild-caught sympatric thick- and thin-lipped cichlids from all four instances of repeated thick-lip evolution. Six genes (apolipoprotein D, myelin-associated glycoprotein precursor, four-and-a-half LIM domain protein 2, calpain-9, GTPase IMAP family member 8-like and one hypothetical protein) are significantly underexpressed in the thick-lipped morph across all four lakes. However, other aspects of lips' gene expression in sympatric morphs differ in a lake-specific pattern, including the magnitude of differentially expressed genes (97-510). Generally, fewer genes are differentially expressed among morphs in the younger crater lakes than in those from the older Great Lakes. Body shape, lower pharyngeal jaw size and shape, and stable isotopes (δ(13)C and δ(15)N) differ between all sympatric morphs, with the greatest differentiation in the Great Lake Nicaragua. Some ecological traits evolve in parallel (those related to foraging ecology; e.g. lip size, body and head shape) but others, somewhat surprisingly, do not (those related to diet and food processing; e.g. jaw size and shape, stable isotopes). Taken together, this case of parallelism among thick- and thin-lipped cichlids shows a mosaic pattern of parallel and nonparallel evolution.

Forschungszusammenhang (Projekte)

    Recknagel, Hans; Elmer, Kathryn R.; Meyer, Axel (2013): A hybrid genetic linkage map of two ecologically and morphologically divergent Midas cichlid fishes (Amphilophus spp.) obtained by massively parallel DNA sequencing (ddRADSeq) G3: Genes, Genomes, Genetics. 2013, 3(1), pp. 65-74. eISSN 2160-1836. Available under: doi: 10.1534/g3.112.003897

A hybrid genetic linkage map of two ecologically and morphologically divergent Midas cichlid fishes (Amphilophus spp.) obtained by massively parallel DNA sequencing (ddRADSeq)

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Cichlid fishes are an excellent model system for studying speciation and the formation of adaptive radiations because of their tremendous species richness and astonishing phenotypic diversity. Most research has focused on African rift lake fishes, although Neotropical cichlid species display much variability as well. Almost one dozen species of the Midas cichlid species complex (Amphilophus spp.) have been described so far and have formed repeated adaptive radiations in several Nicaraguan crater lakes. Here we apply double-digest restriction-site associated DNA sequencing to obtain a high-density linkage map of an interspecific cross between the benthic Amphilophus astorquii and the limnetic Amphilophus zaliosus, which are sympatric species endemic to Crater Lake Apoyo, Nicaragua. A total of 755 RAD markers were genotyped in 343 F(2) hybrids. The map resolved 25 linkage groups and spans a total distance of 1427 cM with an average marker spacing distance of 1.95 cM, almost matching the total number of chromosomes (n = 24) in these species. Regions of segregation distortion were identified in five linkage groups. Based on the pedigree of parents to F(2) offspring, we calculated a genome-wide mutation rate of 6.6 × 10(-8) mutations per nucleotide per generation. This genetic map will facilitate the mapping of ecomorphologically relevant adaptive traits in the repeated phenotypes that evolved within the Midas cichlid lineage and, as the first linkage map of a Neotropical cichlid, facilitate comparative genomic analyses between African cichlids, Neotropical cichlids and other teleost fishes.

Forschungszusammenhang (Projekte)

    Kautt, Andreas F.; Elmer, Kathryn R.; Meyer, Axel (2012): Genomic signatures of divergent selection and speciation patterns in a 'natural experiment', the young parallel radiations of Nicaraguan crater lake cichlid fishes Molecular Ecology. 2012, 21(19), pp. 4770-4786. ISSN 0962-1083. eISSN 1365-294X. Available under: doi: 10.1111/j.1365-294X.2012.05738.x

Genomic signatures of divergent selection and speciation patterns in a 'natural experiment', the young parallel radiations of Nicaraguan crater lake cichlid fishes

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Divergent selection is the main driving force in sympatric ecological speciation and may also play a strong role in divergence between allopatric populations. Characterizing the genome-wide impact of divergent selection often constitutes a first step in unravelling the genetic bases underlying adaptation and ecological speciation. The Midas cichlid fish (Amphilophus citrinellus) species complex in Nicaragua is a powerful system for studying evolutionary processes. Independent colonizations of isolated young crater lakes by Midas cichlid populations from the older and great lakes of Nicaragua resulted in the repeated evolution of adaptive radiations by intralacustrine sympatric speciation. In this study we performed genome scans on two repeated radiations of crater lake species and their great lake source populations (1030 polymorphic AFLPs, n ∼ 30 individuals per species). We detected regions under divergent selection (0.3% in the crater lake Xiloá flock and 1.7% in the older crater lake Apoyo radiation) that might be responsible for the sympatric diversifications. We find no evidence that the same genomic regions have been involved in the repeated evolution of parallel adaptations across crater lake flocks. However, there is some genetic parallelism apparent (seven out of 51 crater lake to great lake outlier loci are shared; 13.7%) that is associated with the allopatric divergence of both crater lake flocks. Interestingly, our results suggest that the number of outlier loci involved in sympatric and allopatric divergence increases over time. A phylogeny based on the AFLP data clearly supports the monophyly of both crater lake species flocks and indicates a parallel branching order with a primary split along the limnetic-benthic axis in both radiations.

Forschungszusammenhang (Projekte)

Mittelgeber
Name Finanzierungstyp Kategorie Kennziffer
Europäische Union Drittmittel Forschungsförderprogramm 526/12
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Laufzeit: 01.10.2012 – 30.09.2017