Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake.
ABSTRACT: The genomic causes and effects of divergent ecological selection during speciation are still poorly understood. Here we report the discovery and detailed characterization of early-stage adaptive divergence of two cichlid fish ecomorphs in a small (700 meters in diameter) isolated crater lake in Tanzania. The ecomorphs differ in depth preference, male breeding color, body shape, diet, and trophic morphology. With whole-genome sequences of 146 fish, we identified 98 clearly demarcated genomic "islands" of high differentiation and demonstrated the association of genotypes across these islands with divergent mate preferences. The islands contain candidate adaptive genes enriched for functions in sensory perception (including rhodopsin and other twilight-vision-associated genes), hormone signaling, and morphogenesis. Our study suggests mechanisms and genomic regions that may play a role in the closely related mega-radiation of Lake Malawi.
Project description: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.
Project description:The polychromatic and trophically polymorphic Midas cichlid fish species complex (Amphilophus cf. citrinellus) is an excellent model system for studying the mechanisms of speciation and patterns of phenotypic diversification in allopatry and in sympatry. Here, we first review research to date on the species complex and the geological history of its habitat. We analyse body shape variation from all currently described species in the complex, sampled from six crater lakes (maximally 1.2-23.9 kyr old) and both great lakes in Nicaragua. We find that Midas cichlid populations in each lake have their own characteristic body shape. In lakes with multiple sympatric species of Midas cichlid, each species has a distinct body shape. Across the species complex, most body shape change relates to body depth, head, snout and mouth shape and caudal peduncle length. There is independent parallel evolution of an elongate limnetic species in at least two crater lakes. Mitochondrial genetic diversity is higher in crater lakes with multiple species. Midas cichlid species richness increases with the size and age of the crater lakes, though no such relationship exists for the other syntopic fishes. We suggest that crater lake Midas cichlids follow the predicted pattern of an adaptive radiation, with early divergence of each crater lake colonization, followed by intralacustrine diversification and speciation by ecological adaptation and sexual selection.
Project description: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. A common pattern of adaptive diversification in freshwater fishes is the repeated evolution of open water (limnetic) species and of shore (benthic) species. Individual specialization can reflect earliest stages of evolutionary and ecological divergence. We here demonstrate individual specialization along the benthic-limnetic axis in a young adaptive radiation of crater lake cichlid fishes.
Project description:<h4>Background</h4>Identifying ecologically significant phenotypic traits and the genomic mechanisms that underly them are crucial steps in understanding traits associated with population divergence. We used genome-wide data to identify genomic regions associated with key traits that distinguish two ecomorphs of rainbow trout (Oncorhynchus mykiss)-insectivores and piscivores-that coexist for the non-breeding portion of the year in Kootenay Lake, southeastern British Columbia. "Gerrards" are large-bodied, rapidly growing piscivores with high metabolic rates that spawn north of Kootenay Lake in the Lardeau River, in contrast to the insectivorous populations that are on average smaller in body size, with lower growth and metabolic rates, mainly forage on aquatic insects, and spawn in tributaries immediately surrounding Kootenay Lake. We used pool-seq data representing ~ 60% of the genome and 80 fish per population to assess the level of genomic divergence between ecomorphs and to identify and interrogate loci that may play functional or selective roles in their divergence.<h4>Results</h4>Genomic divergence was high between sympatric insectivores and piscivores ([Formula: see text] = 0.188), and in fact higher than between insectivorous populations from Kootenay Lake and the Blackwater River ([Formula: see text] = 0.159) that are > 500 km apart. A window-based [Formula: see text] analysis did not reveal "islands" of genomic differentiation; however, the window with highest [Formula: see text] estimate did include a gene associated with insulin secretion. Although we explored the use of the "Local score" approach to identify genomic outlier regions, this method was ultimately not used because simulations revealed a high false discovery rate (~ 20%). Gene ontology (GO) analysis identified several growth processes as enriched in genes occurring in the ~ 200 most divergent genomic windows, indicating many loci of small effect involved in growth and growth-related metabolic processes are associated with the divergence of these ecomorphs.<h4>Conclusion</h4>Our results reveal a high degree of genomic differentiation between piscivorous and insectivorous populations and indicate that the large body piscivorous phenotype is likely not due to one or a few loci of large effect. Rather, the piscivore phenotype may be controlled by several loci of small effect, thus highlighting the power of whole-genome resequencing in identifying genomic regions underlying population-level phenotypic divergences.
Project description:High-throughput culturing (HTC) methods that rely on dilution to extinction in very-low-nutrient media were used to obtain bacterial isolates from Crater Lake, Oregon. 16S rRNA sequence determination and phylogenetic reconstruction were used to determine the potential ecological significance of isolated bacteria, both in Crater Lake and globally. Fifty-five Crater Lake isolates yielded 16 different 16S rRNA gene sequences. Thirty of 55 (55%) Crater Lake isolates had 16S rRNA gene sequences with 97% or greater similarity to sequences recovered previously from Crater Lake 16S rRNA gene clone libraries. Furthermore, 36 of 55 (65%) Crater Lake isolates were found to be members of widely distributed freshwater groups. These results confirm that HTC is a significant improvement over traditional isolation techniques that tend to enrich for microorganisms that do not predominate in their environment and rarely correlate with 16S rRNA gene clone library sequences. Although all isolates were obtained under dark, heterotrophic growth conditions, 2 of the 16 different groups showed evidence of photosynthetic capability as assessed by the presence of puf operon sequences, suggesting that photoheterotrophy may be a significant process in this oligotrophic, freshwater habitat.
Project description:<h4>Background</h4>After a volcano erupts, a lake may form in the cooled crater and become an isolated aquatic ecosystem. This makes fishes in crater lakes informative for understanding sympatric evolution and ecological diversification in barren environments. From a geological and limnological perspective, such research offers insight about the process of crater lake ecosystem establishment and speciation. In the present study we use genetic and coalescence approaches to infer the colonization history of Midas cichlid fishes (Amphilophus cf. citrinellus) that inhabit a very young crater lake in Nicaragua-the ca. 1800 year-old Lake Apoyeque. This lake holds two sympatric, endemic morphs of Midas cichlid: one with large, hypertrophied lips (approximately 20% of the total population) and another with thin lips. Here we test the associated ecological, morphological and genetic diversification of these two morphs and their potential to represent incipient speciation.<h4>Results</h4>Gene coalescence analyses [11 microsatellite loci and mitochondrial DNA (mtDNA) sequences] suggest that crater lake Apoyeque was colonized in a single event from the large neighbouring great lake Managua only about 100 years ago. This founding in historic times is also reflected in the extremely low nuclear and mitochondrial genetic diversity in Apoyeque. We found that sympatric adult thin- and thick-lipped fishes occupy distinct ecological trophic niches. Diet, body shape, head width, pharyngeal jaw size and shape and stable isotope values all differ significantly between the two lip-morphs. The eco-morphological features pharyngeal jaw shape, body shape, stomach contents and stable isotopes (delta15N) all show a bimodal distribution of traits, which is compatible with the expectations of an initial stage of ecological speciation under disruptive selection. Genetic differentiation between the thin- and thick-lipped population is weak at mtDNA sequence (FST = 0.018) and absent at nuclear microsatellite loci (FST < 0.001).<h4>Conclusions</h4>This study provides empirical evidence of eco-morphological differentiation occurring very quickly after the colonization of a new and vacant habitat. Exceptionally low levels of neutral genetic diversity and inference from coalescence indicates that the Midas cichlid population in Apoyeque is much younger (ca. 100 years or generations old) than the crater itself (ca. 1 800 years old). This suggests either that the crater remained empty for many hundreds of years after its formation or that remnant volcanic activity prevented the establishment of a stable fish population during the early life of the crater lake. Based on our findings of eco-morphological variation in the Apoyeque Midas cichlids, and known patterns of adaptation in Midas cichlids in general, we suggest that this population may be in a very early stage of speciation (incipient species), promoted by disruptive selection and ecological diversification.
Project description:Polar regions are characterized by acute seasonal changes in the environment, with organisms inhabiting these regions lacking diel photoperiodic information for parts of the year. We present, to our knowledge, the first high-resolution analysis of diel and seasonal activity of free-living fishes in polar waters (74°N), subject to extreme variation in photoperiod, temperature and food availability. Using biotelemetry, we tracked two sympatric ecomorphs of lake-dwelling Arctic charr (Salvelinus alpinus n = 23) over an annual cycle. Charr activity rhythms reflected the above-surface photoperiod (including under ice), with diel rhythms of activity observed. During the dark winter solstice period, charr activity became arrhythmic and much reduced, even though estimated light levels were within those at which charr can feed. When twilight resumed, charr activity ensued as diel vertical migration, which continued throughout spring and with increasing day length, despite stable water temperatures. Diel activity rhythms ceased during the polar day, with a sharp increase in arrhythmic fish activity occurring at ice-break. Despite contrasting resource use, circannual rhythms were mirrored in the two ecomorphs, although individual variability in activity rhythms was evident. Our data support conclusions of functionally adaptive periods of arrhythmicity in polar animals, suggesting maintenance of a circannual oscillator for scheduling seasonal behavioural and developmental processes.
Project description:Parallel adaptive radiations have arisen following the colonization of islands by lizards and lakes by fishes. In these classic examples, parallel adaptive radiation is a response to the ecological opportunities afforded by the colonization of novel ecosystems and similar adaptive landscapes that favour the evolution of similar suites of ecomorphs, despite independent evolutionary histories. Here, we demonstrate that parallel adaptive radiations of cichlid fishes arose in South American rivers. Speciation-assembled communities of pike cichlids (Crenicichla) have independently diversified into similar suites of novel ecomorphs in the Uruguay and Paraná Rivers, including crevice feeders, periphyton grazers and molluscivores. There were bursts in phenotypic evolution associated with the colonization of each river and the subsequent expansion of morphospace following the evolution of the ecomorphs. These riverine clades demonstrate that characteristics emblematic of textbook parallel adaptive radiations of island- and lake-dwelling assemblages are feasible evolutionary outcomes even in labile ecosystems such as rivers.
Project description: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.
Project description: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.