Contrasting signatures of genomic divergence during sympatric speciation.

The transition from 'well-marked varieties' of a single species into 'well-defined species'-especially in the absence of geographic barriers to gene flow (sympatric speciation)-has puzzled evolutionary biologists ever since Darwin1,2. Gene flow counteracts the buildup of genome-wide differentiation, which is a hallmark of speciation and increases the likelihood of the evolution of irreversible reproductive barriers (incompatibilities) that complete the speciation process3. Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs4, but empirical tests of this theory are scant because comprehensive data are difficult to collect and synthesize across species, owing to their unique biologies and evolutionary histories5. Here, within a young species complex of neotropical cichlid fishes (Amphilophus spp.), we analysed genomic divergence among populations and species. By generating a new genome assembly and re-sequencing 453 genomes, we uncovered the genetic architecture of traits that have been suggested to be important for divergence. Species that differ in monogenic or oligogenic traits that affect ecological performance and/or mate choice show remarkably localized genomic differentiation. By contrast, differentiation among species that have diverged in polygenic traits is genomically widespread and much higher overall, consistent with the evolution of effective and stable genome-wide barriers to gene flow. Thus, we conclude that simple trait architectures are not always as conducive to speciation with gene flow as previously suggested, whereas polygenic architectures can promote rapid and stable speciation in sympatry.

Expansion and Functional Diversification of Long-Wavelength-Sensitive Opsin in Anabantoid Fishes.

Gene duplication is one of the most important sources of novel genotypic diversity and the subsequent evolution of phenotypic diversity. Determining the evolutionary history and functional changes of duplicated genes is crucial for a comprehensive understanding of adaptive evolution. The evolutionary history of visual opsin genes is very dynamic, with repeated duplication events followed by sub- or neofunctionalization. While duplication of the green-sensitive opsins rh2 is common in teleost fish, fewer cases of multiple duplication events of the red-sensitive opsin lws are known. In this study, we investigate the visual opsin gene repertoire of the anabantoid fishes, focusing on the five lws opsin genes found in the genus Betta. We determine the evolutionary history of the lws opsin gene by taking advantage of whole-genome sequences of nine anabantoid species, including the newly assembled genome of Betta imbellis. Our results show that at least two independent duplications of lws occurred in the Betta lineage. The analysis of amino acid sequences of the lws paralogs of Betta revealed high levels of diversification in four of the seven transmembrane regions of the lws protein. Amino acid substitutions at two key-tuning sites are predicted to lead to differentiation of absorption maxima (λmax) between the paralogs within Betta. Finally, eye transcriptomics of B. splendens at different developmental stages revealed expression shifts between paralogs for all cone opsin classes. The lws genes are expressed according to their relative position in the lws opsin cluster throughout ontogeny. We conclude that temporal collinearity of lws expression might have facilitated subfunctionalization of lws in Betta and teleost opsins in general.

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.

Genetic assimilation and the evolution of direction of genital asymmetry in anablepid fishes.

Phylogenetic comparative studies suggest that the direction of deviation from bilateral symmetry (sidedness) might evolve through genetic assimilation; however, the changes in sidedness inheritance remain largely unknown. We investigated the evolution of genital asymmetry in fish of the family Anablepidae, in which males' intromittent organ (the gonopodium, a modified anal fin) bends asymmetrically to the left or the right. In most species, males show a 1 : 1 ratio of left-to-right-sided gonopodia. However, we found that in three species left-sided males are significantly more abundant than right-sided ones. We mapped sidedness onto a new molecular phylogeny, finding that this left-sided bias likely evolved independently three times. Our breeding experiment in a species with an excess of left-sided males showed that sires produced more left-sided offspring independently of their own sidedness. We propose that sidedness might be inherited as a threshold trait, with different thresholds across species. This resolves the apparent paradox that, while there is evidence for the evolution of sidedness, commonly there is a lack of support for its heritability and no response to artificial selection. Focusing on the heritability of the left : right ratio of offspring, rather than on individual sidedness, is key for understanding how the direction of asymmetry becomes genetically assimilated.

A genetically based ecological trade-off contributes to setting a geographic range limit.

Understanding the ecological factors that shape geographic range limits and the evolutionary constraints that prevent populations from adaptively evolving beyond these limits is an unresolved question. Here, we investigated why the euryhaline fish, Poecila reticulata, is confined to freshwater within its native range, despite being tolerant of brackish water. We hypothesised that competitive interactions with a close relative, Poecilia picta, in brackish water prevents P. reticulata from colonising brackish water. Using a combination of field transplant, common garden breeding, and laboratory behaviour experiments, we find support for this hypothesis, as P. reticulata are behaviourally subordinate and have lower survival in brackish water with P. picta. We also found a negative genetic correlation between P. reticulata growth in brackish water versus freshwater in the presence of P. picta, suggesting a genetically based trade-off between salinity tolerance and competitive ability could constrain adaptive evolution at the range limit.

Environmental Change, If Unaccounted, Prevents Detection of Cryptic Evolution in a Wild Population.

AbstractDetecting contemporary evolution requires demonstrating that genetic change has occurred. Mixed effects models allow estimation of quantitative genetic parameters and are widely used to study evolution in wild populations. However, predictions of evolution based on these parameters frequently fail to match observations. Here, we applied three commonly used quantitative genetic approaches to predict the evolution of size at maturity in a wild population of Trinidadian guppies. Crucially, we tested our predictions against evolutionary change observed in common-garden experiments performed on samples from the same population. We show that standard quantitative genetic models underestimated or failed to detect the cryptic evolution of this trait as demonstrated by the common-garden experiments. The models failed because (1) size at maturity and fitness both decreased with increases in population density, (2) offspring experienced higher population densities than their parents, and (3) selection on size was strongest at high densities. When we accounted for environmental change, predictions better matched observations in the common-garden experiments, although substantial uncertainty remained. Our results demonstrate that predictions of evolution are unreliable if environmental change is not appropriately captured in models.

Diversity in visual sensitivity across Neotropical cichlid fishes via differential expression and intraretinal variation of opsin genes.

The visual system of vertebrates has greatly contributed to our understanding of how different molecular mechanisms shape adaptive phenotypic diversity. Extensive work on African cichlid fishes has shown how variation in opsin gene expression mediates diversification as well as convergent evolution in colour vision. This trait has received less attention in Neotropical cichlids, the sister lineage to African cichlids, but the work done so far led to the conclusion that colour vision is much less variable in Neotropical species. However, as only few taxa have been investigated and as recent work found contradicting patterns, the diversity in meotropical cichlids might be greatly underestimated. Here, we survey patterns of opsin gene expression in 35 representative species of Neotropical cichlids, revealing much more variation than previously known. This diversity can be attributed to two main mechanisms: (i) differential expression of the blue-sensitive sws2a, the green-sensitive rh2a, and the red-sensitive lws opsin genes, and (ii) simultaneous expression of up to five opsin genes, instead of only three as commonly found, in a striking dorsoventral pattern across the retina. This intraretinal variation in opsin genes expression results in steep gradients in visual sensitivity that may represent a convergent adaptation to clear waters with broad light environments. These results highlight the role and flexibility of gene expression in generating adaptive phenotypic diversification.

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

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.

Habitat light sets the boundaries for the rapid evolution of cichlid fish vision, while sexual selection can tune it within those limits.

Cichlid fishes' famous diversity in body coloration is accompanied by a highly diverse and complex visual system. Although cichlids possess an unusually high number of seven cone opsin genes, they express only a subset of these during their ontogeny, accounting for their astonishing interspecific variation in visual sensitivities. Much of this diversity is thought to have been shaped by natural selection as cichlids inhabit a variety of habitats with distinct light environments. Also, sexual selection might have contributed to the observed visual diversity, and sexual dimorphism in coloration potentially co-evolved with sexual dimorphism in opsin expression. We investigated sex-specific opsin expression of several cichlids from Africa and the Neotropics and collected and integrated data sets on sex-specific body coloration, species-specific visual sensitivities, lens transmission and habitat light properties for some of them. We comparatively analysed this wide range of molecular and ecological data, illustrating how integrative approaches can address specific questions on the factors and mechanisms driving diversification, and the evolution of cichlid vision in particular. We found that both sexes expressed opsins at the same levels-even in sexually dimorphic cichlid species-which argues against coevolution of sexual dichromatism and differences in sex-specific visual sensitivity. Rather, a combination of environmental light properties and body coloration shaped the diversity in spectral sensitivities among cichlids. We conclude that although cichlids are particularly colourful and diverse and often sexually dimorphic, it would appear that natural rather than sexual selection is a more powerful force driving visual diversity in this hyperdiverse lineage.

Eco-Evolutionary Feedbacks Predict the Time Course of Rapid Life-History Evolution.

Organisms can change their environment and in doing so change the selection they experience and how they evolve. Population density is one potential mediator of such interactions because high population densities can impact the ecosystem and reduce resource availability. At present, such interactions are best known from theory and laboratory experiments. Here we quantify the importance of such interactions in nature by transplanting guppies from a stream where they co-occur with predators into tributaries that previously lacked both guppies and predators. If guppies evolve solely because of the immediate reduction in mortality rate, the strength of selection and rate of evolution should be greatest at the outset and then decline as the population adapts to its new environment. If indirect effects caused by the increase in guppy population density in the absence of predation prevail, then there should be a lag in guppy evolution because time is required for them to modify their environment. The duration of this lag is predicted to be associated with the environmental modification caused by guppies. We observed a lag in life-history evolution associated with increases in population density and altered ecology. How guppies evolved matched predictions derived from evolutionary theory that incorporates such density effects.