Lake Cichlids Research Articles

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

AbstractSelection 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 nonheritable environmentally induced variation. Disentangling these sources of phenotypic variation requires studying closely related populations in nature and in 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 variation in visual sensitivities 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.

Social deprivation in maternal mouthbrooders Tropheus sp. “Caramba” (Teleostei: Cichlidae) decreases the success rate of reproduction and survival rate of fish fry

Early offspring separation from mothers causes social deprivation. Mouthbrooding, when eggs and fry are incubated in the buccal cavity of the parent, is one of the reproductive strategies in fish. The mother is the incubating parent in African lake cichlids from the genus Tropheus. Many of these are produced in captivity and some producers use artificial incubators in which eggs are incubated separately from the mother. We hypothesized that this practice may dramatically modify the reproduction rate of fish individuals produced by the method of artificial incubation. The long-term experiment focused on Tropheus sp. “Caramba” had been carried out for 10 years when maternally incubated and separated individuals were compared. We found a negative effect of artificial egg and offspring incubation out of the mother’s buccal cavity. The deprived females laid the same number of eggs as maternally incubated females, but most eggs were lost during the incubation. Moreover, the reproduction frequency was significantly lower in deprived females in comparison with those maternally incubated. This study should be perceived as preliminary. For this reason and with respect to welfare principles, we strongly recommend similarly designed experiments focused on other potentially sensitive fish mouthbrooders. Once the syndrome would be confirmed, we recommend avoiding artificial incubation of mouthbrooding fish in general.

Sympatric and allopatric Alcolapia soda lake cichlid species show similar levels of assortative mating

Characterizing reproductive barriers such as mating preferences within rapid evolutionary radiations is crucial for understanding the early stages of speciation. Cichlid fishes are well-known for their adaptive radiations and capacity for rapid speciation and as such we investigate assortative mating among Alcolapia species; a recent (<10,000 years), small adaptive radiation, endemic to the extreme soda lakes, Magadi (one species) and Natron (three species), in East Africa. In seminatural aquarium conditions, we observed both courtship and mate choice (tested by microsatellite paternity analysis) to be significantly assortative among the three sympatric Natron species in a three-way choice experiment. This was also the case between allopatric species from Natron and Magadi, as found in a two-way choice experiment. However, the proportion of disassortative matings was substantial in both of these experiments, with hybrids comprising 29% of offspring in sympatric species and 11.4% in allopatric species comparisons. Previous work suggests that the Natron/Magadi split might not be much older than the radiation within Natron, so the similar rate of hybridization in the allopatric comparison is surprising and inconsistent with predictions of reinforcement theory, which predicts a faster rate of accumulation of premating isolation in sympatry. The relatively weak assortative mating in sympatry suggests that additional reproductive barriers, such as microhabitat preferences or spatial structuring may contribute to genetic isolation in nature.

Early stages of sympatric homoploid hybrid speciation in crater lake cichlid fishes

Homoploid hybrid speciation (i.e., hybrid speciation without a change in ploidy) has traditionally been considered to be rare in animals. Only few accepted empirical examples of homoploid hybrid speciation in nature exist, and in only one previous case (insects) was it convincingly shown that this process occurred in complete sympatry. Here, we report an instance of sympatric homoploid hybrid speciation in Midas cichlid fishes in Crater Lake Xiloá, Nicaragua. The hybrid lineage, albeit at an early stage of speciation, has genomically and phenotypically diverged from both of its two parental species. Together with a distinct stable isotope signature this suggests that this hybrid lineages occupies a different trophic niche compared to the other sympatric Midas cichlid species in Crater Lake Xiloá.

A method for quick and efficient identification of cichlid species by high resolution DNA melting analysis of minibarcodes

Freshwater bodies are key in supporting aquatic and terrestrial life. Ecological balance of freshwater habitats is very vulnerable, hence, often significantly disrupted by climatic changes and anthropogenic acts. In Israel, due to its relatively arid climate, many freshwater resources have been disrupted and still are under great pressure. The Sea of Galilee is the largest surface freshwater body in the Middle East and a habitat to unique populations of several fishes, including six cichlid species. Studies on the ecology of these fish and their conservation require effective monitoring tools. In this study, a simple and efficient molecular method was developed to identify the species of these lake cichlids using high resolution melting analysis of mini DNA barcodes. The species of an individual sample can be identified by a single tube PCR reaction. This assay successfully identified sequence differences both among and within species. Here, this method identified the species for 279 small cichlid fry that could not be morphologically identified, allowing to estimate relative species abundance and map their distribution in time and location. The results are key to understand not only the ecology of young stages but also their recruitment potential to adult fish populations and their sustainability. This method can be readily implemented in further ecological studies and surveys related to these species, in the lake and its surroundings, as a tool to enhance understanding and protection of these species.

The comparative genomic landscape of adaptive radiation in crater lake cichlid fishes.

Factors ranging from ecological opportunity to genome composition might explain why only some lineages form adaptive radiations. While being rare, particular systems can provide natural experiments within an identical ecological setting where species numbers and phenotypic divergence in two closely related lineages are notably different. We investigated one such natural experiment using two de novo assembled and 40 resequenced genomes and asked why two closely related Neotropical cichlid fish lineages, the Amphilophus citrinellus species complex (Midas cichlids; radiating) and Archocentrus centrarchus (Flyer cichlid; nonradiating), have resulted in such disparate evolutionary outcomes. Although both lineages inhabit many of the same Nicaraguan lakes, whole‐genome inferred demography suggests that priority effects are not likely to be the cause of the dissimilarities. Also, genome‐wide levels of selection, transposable element dynamics, gene family expansion, major chromosomal rearrangements and the number of genes under positive selection were not markedly different between the two lineages. To more finely investigate particular subsets of the genome that have undergone adaptive divergence in Midas cichlids, we also examined if there was evidence for ‘molecular pre‐adaptation’ in regions identified by QTL mapping of repeatedly diverging adaptive traits. Although most of our analyses failed to pinpoint substantial genomic differences, we did identify functional categories containing many genes under positive selection that provide candidates for future studies on the propensity of Midas cichlids to radiate. Our results point to a disproportionate role of local, rather than genome‐wide factors underlying the propensity for these cichlid fishes to adaptively radiate.

Analysis of structural variants in four African cichlids highlights an association with developmental and immune related genes

BackgroundEast African lake cichlids are one of the most impressive examples of an adaptive radiation. Independently in Lake Victoria, Tanganyika, and Malawi, several hundreds of species arose within the last 10 million to 100,000 years. Whereas most analyses in cichlids focused on nucleotide substitutions across species to investigate the genetic bases of this explosive radiation, to date, no study has investigated the contribution of structural variants (SVs) in the evolution of adaptive traits across the three Great Lakes of East Africa.ResultsHere, we annotate and characterize the repertoires and evolutionary potential of different SV classes (deletion, duplication, inversion, insertions and translocations) in four cichlid species: Haplochromis burtoni, Metriaclima zebra, Neolamprologus brichardi and Pundamilia nyererei. We investigate the patterns of gain and loss evolution for each SV type, enabling the identification of lineage specific events. Both deletions and inversions show a significant overlap with SINE elements, while inversions additionally show a limited, but significant association with DNA transposons. Inverted regions are enriched for genes regulating behaviour, or involved in skeletal and visual system development. We also find that duplicated regions show enrichment for genes associated with “antigen processing and presentation” and other immune related categories. Our pipeline and results were further tested by PCR validation of selected deletions and inversions, which confirmed respectively 7 out of 10 and 6 out of 9 events.ConclusionsAltogether, we provide the first comprehensive overview of rearrangement evolution in East African cichlids, and some important insights into their likely contribution to adaptation.

Diving into divergence: Differentiation in swimming performances, physiology and gene expression between locally-adapted sympatric cichlid fishes.

Sympatric speciation occurs without geographical barriers and is thought to often be driven by ecological specialization of individuals that eventually diverge genetically and phenotypically. Distinct morphologies between sympatric populations occupying different niches have been interpreted as such differentiating adaptive phenotypes, yet differences in performance and thus likely adaptiveness between them were rarely tested. Here, we investigated if divergent body shapes of two sympatric crater lake cichlid species from Nicaragua, one being a shore-associated (benthic) species while the other prefers the open water zones (limnetic), affect cruising (Ucrit ) and sprinting (Usprint ) swimming abilities - performances particularly relevant to their respective lifestyles. Furthermore, we investigated species differences in oxygen consumption (MO2 ) across different swimming speeds and compare gene expression in gills and white muscle at rest and during exercise. We found a superior cruising ability in the limnetic Amphilophus zaliosus compared to the benthic Amphilophus astorquii, while sprinting was not different, suggesting that their distinct morphologies affect swimming performance. Increased cruising swimming ability in A.zaliosus was linked to a higher oxygen demand during activity (but not rest), indicating different metabolic rates during exercise - a hypothesis supported by coinciding gene expression patterns of gill transcriptomes. We identified differentially expressed genes linked to swimming physiology, regulation of swimming behaviour and oxygen intake. A combination of physiological and morphological differences may thus underlie adaptations to these species' distinct niches. This complex ecological specialization probably resulted in morphological and physiological trade-offs that contributed to the rapid establishment and maintenance of divergence with gene flow.

MicroRNA Gene Regulation in Extremely Young and Parallel Adaptive Radiations of Crater Lake Cichlid Fish.

Cichlid fishes provide textbook examples of explosive phenotypic diversification and sympatric speciation, thereby making them ideal systems for studying the molecular mechanisms underlying rapid lineage divergence. Despite the fact that gene regulation provides a critical link between diversification in gene function and speciation, many genomic regulatory mechanisms such as microRNAs (miRNAs) have received little attention in these rapidly diversifying groups. Therefore, we investigated the posttranscriptional regulatory role of miRNAs in the repeated sympatric divergence of Midas cichlids (Amphilophus spp.) from Nicaraguan crater lakes. Using miRNA and mRNA sequencing of embryos from five Midas species, we first identified miRNA binding sites in mRNAs and highlighted the presences of a surprising number of novel miRNAs in these adaptively radiating species. Then, through analyses of expression levels, we identified putative miRNA/gene target pairs with negatively correlated expression level that were consistent with the role of miRNA in downregulating mRNA. Furthermore, we determined that several miRNA/gene pairs show convergent expression patterns associated with the repeated benthic/limnetic sympatric species divergence implicating these miRNAs as potential molecular mechanisms underlying replicated sympatric divergence. Finally, as these candidate miRNA/gene pairs may play a central role in phenotypic diversification in these cichlids, we characterized the expression domains of selected miRNAs and their target genes via in situ hybridization, providing further evidence that miRNA regulation likely plays a role in the Midas cichlid adaptive radiation. These results provide support for the hypothesis that extremely quickly evolving miRNA regulation can contribute to rapid evolutionary divergence even in the presence of gene flow.

Molecular basis of adaptation to hypoxia in Barombi Mbo crater lake cichlids

Event Abstract Back to Event Molecular basis of adaptation to hypoxia in Barombi Mbo crater lake cichlids Dmytro Omelchenko1*, Pavel Talacko1, Adrian Indermaur2, Walter Salzburger2 and Zuzana Musilova1 1 Charles University, Czechia 2 University of Basel, Switzerland Deep water zone represents an extreme environment where organisms have to cope with low dissolved oxygen concentrations, low-intensity light with the narrower color spectrum and high hydrostatic pressure. Such conditions create selective pressure and shape the evolution of living organisms in deep waters. They establish various adaptations to exploit energy sources which are unavailable for shallow-water inhabitants. The general challenge of adaptation research is to identify the link between the species ecology, environment and the molecular adaptation in different species. Here we study endemic cichlid fishes from the crater lake Barombi Mbo in Cameroon, West Africa. We compare shallow-water and deep-water cichlid species from monophyletic species flock focusing on gene sequence, expression levels and proteome abundance of hemoglobins and other candidate proteins (myoglobin, coagulation factors) that might be involved in establishment of adaptation to life in the depth. We performed genome assembly of 4 Barombi Mbo cichlid species and obtained information about exact synteny of hemoglobin gene clusters. We inferred CDS structure of hemoglobin genes with subsequent phylogenetic analysis. In addition, we inspected the hemoglobin clusters in the closely related species, Nile tilapia, and identified 17 Hb-alpha and 15 Hb-beta genes. According to our knowledge Nile Tilapia has the highest number of hemoglobin genes among Vertebrates. Furthermore, we performed RNA sequencing of the gill tissue and calculated gene expression for hemoglobin subunits. We estimated that from multiple hemoglobin genes (18 in Barombi Mbo cichlids) only four are expressed in adult fish. We observed that those are two pairs of alpha and beta subunits which are located in the close synteny. We further estimated that expression in deep-water species is slightly higher and favored towards one pair of the hemoglobin genes while in shallow-water species expression is shifted towards another pair of hemoglobin subunit genes. This might be connected to our observation that allele of the genes (Hb-beta 11 and Hb-alpha 12) that have higher expression in two deep-water species possessing 4 amino acid substitutions (3 in Hb-beta 11 and 1 in Hb-alpha 12 respectively). Moreover, we performed targeted and non-targeted HPLC-MS/MS analysis of blood proteome and identified 23 proteins that are differentially abundant in fishes coming from different depth horizons. We demonstrate that adaptation to hypoxia in Barombi Mbo crater lake cichlids is likely reflected on several levels including structural changes within coding region of hemoglobin genes and their expression. In addition, we provide evidence of engagement of various proteins in hypoxia adaptation. Keywords: Cichlids, Hemoglobin, hypoxia, Proteome, adaptation, Differential gene expression, crater lake Conference: XVI European Congress of Ichthyology, Lausanne, Switzerland, 2 Sep - 6 Sep, 2019. Presentation Type: Oral Topic: GENETICS, GENOMICS AND PHYSIOLOGY Citation: Omelchenko D, Talacko P, Indermaur A, Salzburger W and Musilova Z (2019). Molecular basis of adaptation to hypoxia in Barombi Mbo crater lake cichlids. Front. Mar. Sci. Conference Abstract: XVI European Congress of Ichthyology. doi: 10.3389/conf.fmars.2019.07.00062 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 21 Jul 2019; Published Online: 14 Aug 2019. * Correspondence: Mr. Dmytro Omelchenko, Charles University, Prague, Czechia, omeldima@gmail.com Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Dmytro Omelchenko Pavel Talacko Adrian Indermaur Walter Salzburger Zuzana Musilova Google Dmytro Omelchenko Pavel Talacko Adrian Indermaur Walter Salzburger Zuzana Musilova Google Scholar Dmytro Omelchenko Pavel Talacko Adrian Indermaur Walter Salzburger Zuzana Musilova PubMed Dmytro Omelchenko Pavel Talacko Adrian Indermaur Walter Salzburger Zuzana Musilova Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

From shallow to deep divergences: mixed messages from Amazon Basin cichlids

Cichlids are a conspicuous component of Amazonian ichthyofauna, filling a wide range of niches. Yet taxonomy of many groups is still poorly known in the Amazon, and most of the yet-to-be discovered species are concentrated there. We analyzed 230 individuals sampled from six major Amazonian River Basins representing 56 morpho-species, 34 nominal and 22 undescribed species in 18 cichlid genera. We used four different single-locus species-discovery (SLSD) methods, delimiting between 53 (mPTP) and 57 (GMYC) species/lineages. When detected, species/lineages are hierarchically geographically structured. Many groups such as the Geophaginae and the Cichlinae have recently diversified, and species of genera such as Cichla and Symphysodon hybridize or have a history of hybridization; thus, these species will not be detected by SLSD methods. At the same time, for example, the genera Apistogramma and Biotodoma harbor cryptic species. For all these reasons, species/lineage diversity of Amazonian cichlids is significantly underestimated. The diversity of Amazonian cichlids is particularly remarkable given that the 570 species of Neotropical cichlids, many of which are from the Amazon Basin, are found in just 1.7% of the freshwater aquatic habitat in which the ~ 2,000 species of the East African rift lake cichlids evolved.

Don't throw out the sympatric speciation with the crater lake water: fine-scale investigation of introgression provides equivocal support for causal role of secondary gene flow in one of the clearest examples of sympatric speciation.

Genomic data has revealed complex histories of colonization and repeated gene flow previously unrecognized in some of the most celebrated examples of sympatric speciation and radiation. However, much of the evidence for secondary gene flow into these radiations comes from summary statistics calculated from sparse genomic sampling without knowledge of which specific genomic regions introgressed. This tells us little about how gene flow potentially influenced sympatric diversification. Here, we investigated whole genomes of Barombi Mbo crater lake cichlids for fine‐scale patterns of introgression with neighboring riverine cichlid populations. We found evidence of secondary gene flow into the radiation scattered across <0.24% of the genome; however, from our analyses, it is not clear if the functional diversity in these regions contributed to the ecological, sexual, and morphological diversity found in the lake. Unlike similar studies, we found no obvious candidate genes for adaptive introgression and we cannot rule out that secondary gene flow was predominantly neutral with respect to the diversification process. We also found evidence for differential assortment of ancestral polymorphisms found in riverine populations between sympatric sister species, suggesting the presence of an ancestral hybrid swarm. Although the history of gene flow and colonization is more complicated than previously assumed, the lack of compelling evidence for secondary gene flow's role in species diversification suggests that we should not yet rule out one of the most celebrated examples of sympatric speciation in nature without a more thorough investigation of the timing and functional role of each introgressed region.

Recent sympatric speciation involving habitat-associated nuptial colour polymorphism in a crater lake cichlid

Even though the idea that modes of speciation other than allopatric speciation are possible in nature is now widespread, compelling examples of ecological speciation in sympatry remain rare. We studied an undescribed radiation of haplochromine cichlids in a young crater lake in western Uganda, and in the small river that is nearby but has currently no known surface connection to the lake. We describe two different modes of speciation that occurred in this cichlid lineage within the past 1,500–10,000 years. Not constrained by gene flow, allopatric divergence between river and lake cichlids affects many different morphological traits as well as nuptial colouration—muted in the river, but intensified and polymorphic in lake cichlids—and neutral genetic differentiation. More surprisingly, we demonstrate a case for sympatric speciation within the small lake that is associated with dramatic differences in male breeding colouration (yellow with bright red-chest versus bright blue) and subtle differences in microhabitat, feeding regime and morphology. Reproductive isolation by assortative mating is suggested by significant differentiation between yellow and blue males in neutral markers of gene flow despite complete sympatry. We hypothesize speciation is mediated by divergent selection on sexual signalling between microhabitats.

Speciation in sympatry with ongoing secondary gene flow and a potential olfactory trigger in a radiation of Cameroon cichlids.

The process of sympatric speciation in nature remains a fundamental unsolved problem. Cameroon crater lake cichlid radiations were long regarded as one of the most compelling examples; however, recent work showed that their origins were more complex than a single colonization event followed by isolation. Here, we performed a detailed investigation of the speciation history of a radiation of Coptodon cichlids from Lake Ejagham, Cameroon, using whole-genome sequencing data. The existence of the Lake Ejagham Coptodon radiation is remarkable as this 0.5km2 lake offers limited scope for divergence across a shallow depth gradient, disruptive selection is currently weak, and the species are sexually monochromatic. We infer that Lake Ejagham was colonized by Coptodon cichlids soon after its formation 9,000years ago, yet speciation occurred only in the last 1,000-2,000years. We show that secondary gene flow from a nearby riverine species has been ongoing, into ancestral as well as extant lineages, and we identify and date river-to-lake admixture blocks. One block contains a cluster of olfactory receptor genes that introgressed near the time of the first speciation event and coincides with a higher overall rate of admixture. Olfactory signalling is a key component of mate choice and species recognition in cichlids. A functional role for this introgression event is consistent with previous findings that sexual isolation appears much stronger than ecological isolation in Ejagham Coptodon. We conclude that speciation in this radiation took place in sympatry, yet may have benefited from ongoing riverine gene flow.

Incipient speciation driven by hypertrophied lips in Midas cichlid fishes?

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.

Molecular characterization of MHC class IIB genes of sympatric Neotropical cichlids

BackgroundThe Major Histocompatibility Complex (MHC) is a key component of the adaptive immune system of all vertebrates and consists of the most polymorphic genes known to date. Due to this complexity, however, MHC remains to be characterized in many species including any Neotropical cichlid fish. Neotropical crater lake cichlids are ideal models to study evolutionary processes as they display one of the most convincing examples of sympatric and repeated parallel radiation events within and among isolated crater lakes.ResultsHere, we characterized the genes of MHC class IIB chain of the Midas cichlid species complex (Amphilophus cf. citrinellus) including fish from five lakes in Nicaragua. We designed 19 new specific primers anchored in a stepwise fashion in order to detect all alleles present. We obtained 866 genomic DNA (gDNA) sequences from thirteen individuals and 756 additional sequences from complementary DNA (cDNA) of seven of those individuals. We identified 69 distinct alleles with up to 25 alleles per individual. We also found considerable intron length variation and mismatches of alleles detected in cDNA and gDNA suggesting that some loci have undergone pseudogenization. Lastly, we created a model of protein structure homology for each allele and identified their key structural components.ConclusionsOverall, the Midas cichlid has one of the most diverse repertoires of MHC class IIB genes known, which could serve as a powerful tool to elucidate the process of divergent radiations, colonization and speciation in sympatry.

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

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.

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

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.

Replicated divergence in cichlid radiations mirrors a major vertebrate innovation.

Decoupling of the upper jaw bones--jaw kinesis--is a distinctive feature of the ray-finned fishes, but it is not clear how the innovation is related to the extraordinary diversity of feeding behaviours and feeding ecology in this group. We address this issue in a lineage of ray-finned fishes that is well known for its ecological and functional diversity--African rift lake cichlids. We sequenced ultraconserved elements to generate a phylogenomic tree of the Lake Tanganyika and Lake Malawi cichlid radiations. We filmed a diverse array of over 50 cichlid species capturing live prey and quantified the extent of jaw kinesis in the premaxillary and maxillary bones. Our combination of phylogenomic and kinematic data reveals a strong association between biting modes of feeding and reduced jaw kinesis, suggesting that the contrasting demands of biting and suction feeding have strongly influenced cranial evolution in both cichlid radiations.

Allopatry, competitor recognition and heterospecific aggression in crater lake cichlids.

BackgroundAggressive behaviour can have significant evolutionary consequences–not only within species, but also in the context of heterospecific interactions. Here, we carried out an experimental field study to investigate the importance of phenotypic similarity on levels of aggression between species whilst controlling for familiarity effects using manipulated allopatric stimuli. Specifically, we investigated aggressive responses of territory holding males and females in two species of Neotropical cichlid fish, Amphilophus sagittae and Hypsophrys nicaraguensis, that differ in their phenotypic similarity to our allopatric stimulus species, Amphilophus astorquii.ResultsWe found that, independent of phenotypic similarity (and correlated phylogenetic proximity) between the territory holders and intruder, territorial aggression was not adjusted in relation to allopatric intruder colour markings that are associated with different levels of threat and known to provoke different responses in a sympatric setting. We also found that males and females did not differ in their overall patterns of aggression adjustment towards intruder cues. Nevertheless, the two focal species, which share the same breeding grounds and external threats, exhibited different sex roles in breeding territory defence.ConclusionTogether with earlier studies assessing hetrospecific aggression in sympatry, our current results highlight the importance of coevolution and learning in species interactions.