Jeffrey S. McKinnon

Speciation in nature: the threespine stickleback model systems

Abstract The threespine stickleback Gasterosteus aculeatus species complex is an important natural model for speciation research because it includes several replicated sets of coexisting, divergent forms that are also experimentally tractable. Recent research has begun to emphasize lesser known divergences within the complex in addition to the well-studied limnetic–benthic pairs, as well as exploring a broader range of speciation mechanisms. With the goals of making general inferences about speciation in nature and bringing this body of research to a wider audience, we have surveyed studies from the entire species complex. We find that stickleback speciation is often rapid, that the geographical context of speciation is variable and often complex, and that many, diverse traits have often diverged early in the speciation process. We find no unambiguous evidence of founder-effect speciation, but much evidence that divergent natural and sexual selection have been central to the evolution of reproductive isolation in this species complex.

Evidence for ecology's role in speciation

A principal challenge in testing the role of natural selection in speciation is to connect the build-up of reproductive isolation between populations to divergence of ecologically important traits. Demonstrations of ‘parallel speciation’, or assortative mating by selective environment, link ecology and isolation, but the phenotypic traits mediating isolation have not been confirmed. Here we show that the parallel build-up of mating incompatibilities between stickleback populations can be largely accounted for by assortative mating based on one trait, body size, which evolves predictably according to environment. In addition to documenting the influence of body size on reproductive isolation for stickleback populations spread across the Northern Hemisphere, we have confirmed its importance through a new experimental manipulation. Together, these results suggest that speciation may arise largely as a by-product of ecological differences and divergent selection on a small number of phenotypic traits.

Parallel Evolution and Inheritance of Quantitative Traits

Parallel phenotypic evolution, the independent evolution of the same trait in closely related lineages, is interesting because it tells us about the contribution of natural selection to phenotypic evolution. Haldane and others have proposed that parallel evolution also results from a second process, the similarly biased production of genetic variation in close relatives, an idea that has received few tests. We suggest that influence of shared genetic biases should be detectable by the disproportionate use of the same genes in independent instances of parallel phenotypic evolution. We show how progress in testing this prediction can be made through simple tests of parallel inheritance of genetic differences: similar additive, dominance, and epistasis components in analysis of line means and similar effective numbers of loci. We demonstrate parallel inheritance in two traits, lateral plate number and body shape, in two lineages of threespine stickleback that have adapted independently to freshwater streams on opposite sides of the Pacific Ocean. Notably, reduction of plate number in freshwater involves a substitution at the same major locus in both lineages. Our results represent only a first step in the study of the genetics of parallel phenotypic evolution in sticklebacks. Nevertheless, we have shown how such studies can be employed to test the genetic hypothesis of parallel evolution and how study of parallel evolution might yield insights into the roles of both selection and genetic constraint in phenotypic evolution.

Colour polymorphism and correlated characters: genetic mechanisms and evolution

Colour polymorphisms (CP’s) continue to be of interest to evolutionary biologists because of their general tractability, importance in studies of selection and potential role in speciation. Since some of the earliest studies of CP, it has been evident that alternative colour morphs often differ in features other than colour. Here we review the rapidly accumulating evidence concerning the genetic mechanisms underlying correlations between CP and other traits in animals. We find that evidence for genetic correlations is now available for taxonomically diverse systems and that physical linkage and regulatory mechanisms including transcription factors, cis‐regulatory elements, and hormone systems provide pathways for the ready accumulation or modification of these correlations. Moreover, physical linkage and regulatory mechanisms may both contribute to genetic correlation in some of the best‐studied systems. These results raise the possibility that negative frequency‐dependent selection and disruptive selection might often be acting on suites of traits and that the cumulative effects of such selection, as well as correlational selection, may be important to CP persistence and evolution. We consider additional evolutionary implications. We recommend continued efforts to elucidate the mechanisms underlying CP‐correlated characters and the more frequent application of comparative approaches, looking at related species that vary in character correlations and patterns of selection. We also recommend efforts to elucidate how frequency‐dependent selection may act on suites of characters.

Colour polymorphism and correlated characters

Colour polymorphisms (CP’s) continue to be of interest to evolutionary biologists because of their general tractability, importance in studies of selection and potential role in speciation. Since some of the earliest studies of CP, it has been evident that alternative colour morphs often differ in features other than colour. Here we review the rapidly accumulating evidence concerning the genetic mechanisms underlying correlations between CP and other traits in animals. We find that evidence for genetic correlations is now available for taxonomically diverse systems and that physical linkage and regulatory mechanisms including transcription factors, cis‐regulatory elements, and hormone systems provide pathways for the ready accumulation or modification of these correlations. Moreover, physical linkage and regulatory mechanisms may both contribute to genetic correlation in some of the best‐studied systems. These results raise the possibility that negative frequency‐dependent selection and disruptive selection might often be acting on suites of traits and that the cumulative effects of such selection, as well as correlational selection, may be important to CP persistence and evolution. We consider additional evolutionary implications. We recommend continued efforts to elucidate the mechanisms underlying CP‐correlated characters and the more frequent application of comparative approaches, looking at related species that vary in character correlations and patterns of selection. We also recommend efforts to elucidate how frequency‐dependent selection may act on suites of characters.

Microhabitat variation and sexual selection can maintain male color polymorphisms.

Abstract Male color polymorphism may be an important precursor to sympatric speciation by sexual selection, but the processes maintaining such polymorphisms are not well understood. Here, we develop a formal model of the hypothesis that male color polymorphisms may be maintained by variation in the sensory environment resulting in microhabitat-specific selection pressures. We analyze the evolution of two male color morphs when color perception (by females and predators) is dependent on the microhabitat in which natural and sexual selection occur. We find that an environment of heterogeneous microhabitats can lead to the maintenance of color polymorphism despite asymmetries in the strengths of natural and sexual selection and in microhabitat proportions. We show that sexual selection alone is sufficient for polymorphism maintenance over a wide range of parameter space, even when female preferences are weak. Polymorphisms can also be maintained by natural selection acting alone, but the conditions for polymorphism maintenance by natural selection will usually be unrealistic for the case of microhabitat variation. Microhabitat variation and sexual selection for conspicuous males may thus provide a situation particularly favorable to the maintenance of male color polymorphisms. These results are important both because of the general insight they provide into a little appreciated mechanism for the maintenance of variation in natural populations and because such variation is an important prerequisite for sympatric speciation.

Environment-contingent sexual selection in a colour polymorphic fish

Sexual selection could be a driving force in the maintenance of intraspecific variation, but supporting observations from nature are limited. Here, we test the hypothesis that spatial heterogeneity of the visual environment can influence sexual selection on colourful male secondary traits such that selective advantage is environment contingent. Using a small fish endemic to Sulawesi, Indonesia (Telmatherina sarasinorum) that has five male colour morphs varying in frequency between two visually distinct mating habitats, we used direct behavioural observations to test the environment-contingent selection hypothesis. These observations were combined with measurements of the visual environment, fish coloration and the sensitivity of visual photopigments to determine whether differential morph conspicuousness was associated with reproductive success across habitats. We found that blue and yellow males are most conspicuous in different habitats, where they also have the highest reproductive fitness. A less conspicuous grey morph also gained high reproductive success in both habitats, raising the possibility that alternative behaviours may also contribute to reproductive success. In a comprehensive analysis, conspicuousness was strongly correlated with reproductive success across morphs and environments. Our results suggest an important role for spatially heterogeneous environments in the maintenance of male colour polymorphism.

Directional sexual selection on chroma and within–pattern colour contrast in Labeotropheus fuelleborni

Speciation via intersexual selection on male nuptial colour pattern is thought to have been a major force in promoting the explosive speciation of African haplochromine cichlids, yet there is very little direct empirical evidence of directional preferences within populations. In this study, we used objective spectrophotometry and analyses based on visual physiology to determine whether females of the Katale population of Labeotropheus fuelleborni, a Lake Malawi haplochromine, prefer males that have higher chroma and more within–pattern colour contrast. In paired male preference tests, female Katale L. fuelleborni showed increasing preferences for males with more relatively saturated colours on their flanks. They also showed increasing preferences for males with relatively higher contrast levels among flank elements. This is the first empirical evidence, to our knowledge, for male colour as a directionally sexually selected trait within a haplochromine cichlid population.

Cuckoldry incites cannibalism: male fish turn to cannibalism when perceived certainty of paternity decreases.

Perceived certainty of paternity is expected to influence a male’s behavior toward his offspring: if he is uncertain of his reproductive success with a current brood due to the presence of cuckolders, it may benefit him to invest instead in future reproduction. A decrease in perceived certainty of paternity incites filial cannibalism (the eating of one’s own offspring) in some teleost fishes that provide parental care; however, no work has demonstrated that cannibalism increases proportionately with increased levels of cuckoldry. Here we show for the first time in a fish with no parental care that as the number of cuckolders at a spawning event increases, so does the probability that a male will cannibalize eggs. In field observations of Telmatherina sarasinorum, a small fish endemic to Sulawesi, Indonesia, males increased filial cannibalism behavior threefold in the presence of one cuckolder and nearly sixfold in the presence of two or more cuckolders. This suggests that males may use detection of cuckolders as an indication that the paternity of current offspring has been compromised.

Reflectance spectra from free-swimming sticklebacks (Gasterosteus): Social context and eye-jaw contrast

Summary The color patterns of many organisms change rapidly with social context but such dynamic signals have been little studied with current methods. In this study we applied objective spectrophotometry techniques to the color displays of unrestrained male threespine sticklebacks, to assess the ine uence of social context on coloration. Analyzing our data with a color space model based on stickleback visual physiology, we found that unrestrained males enhanced saturation of both their blue eye and red jaw color in response to the presence of a mature male or female conspecie c. Divergence between the eye and the jaw lead to enhanced contrast, likely increasing conspicuousness. We found little relationship between measures of color saturation and condition, but the color of males in better condition varied more with social context. This study is the e rst to evaluate contrast between stickleback color pattern elements quantitatively and the e rst in which ree ectance spectra were collected from freeswimming e sh. The methods presented here could be used in future studies of sticklebacks and could potentially be adapted to other animals.