Sympatric colour polymorphisms associated with nonrandom gene flow in cichlid fish of Lake Victoria

Colour polymorphisms have fascinated evolutionary ecologists for a long time. Yet, knowledge on the mechanisms that allow their persistence is restricted to a handful of well-studied cases. We studied two species of Lake Victoria cichlid fish, Neochromis omnicaeruleus and Neochromis greenwoodi, exhibiting very similar sex-linked colour polymorphisms. The ecology and behaviour of one of these species is well studied, with colour-based mating and aggression preferences. Here, we ask whether the selection potentially resulting from female and male mating preferences and aggression biases reduces gene flow between the colour morphs and permits differentiation in traits other than colour. Over the past 14 years, the frequencies of colour morphs have somewhat oscillated, but there is no evidence for directional change, suggesting the colour polymorphism is persistent on an ecological timescale. We find limited evidence of ecomorphological differentiation between sympatric ancestral (plain) and derived (blotched) colour morphs. We also find significantly nonrandom genotypic assignment and an excess of linkage disequilibrium in the plain morph, which together with previous information on mating preferences suggests nonrandom mating between colour morphs. This, together with negative frequency-dependent sexual selection, found in previous studies, may facilitate maintenance of these polymorphisms in sympatry

A Method for Detecting Population Genetic Structure in Diverse, High Gene-Flow Species

Detecting small amounts of genetic subdivision across geographic space remains a persistent challenge. Often a failure to detect genetic structure is mistaken for evidence of panmixia, when more powerful statistical tests may uncover evidence for subtle geographic differentiation. Such slight subdivision can be demographically and evolutionarily important as well as being critical for management decisions. We introduce here a method, called spatial analysis of shared alleles (SAShA), that detects geographically restricted alleles by comparing the spatial arrangement of allelic co-occurrences with the expectation under panmixia. The approach is allele-based and spatially explicit, eliminating the loss of statistical power that can occur with user-defined populations and statistical averaging within populations. Using simulated data sets generated under a stepping-stone model of gene flow, we show that this method outperforms spatial autocorrelation (SA) and UST under common real-world conditions: at relatively high migration rates when diversity is moderate or high, especially when sampling is poor. We then use this method to show clear differences in the genetic patterns of 2 nearshore Pacific mollusks, Tegula funebralis (5 Chlorostoma funebralis) and Katharina tunicata, whose overall patterns of within-species differentiation are similar according to traditional population genetics analyses. SAShA meaningfully complements UST/FST, SA, and other existing geographic genetic analyses and is especially appropriate for evaluating species with high gene flow and subtle genetic differentiation.

Community Genetics Reveal Elevated Levels of Sympatric Gene Flow among Morphologically Similar but Not among Morphologically Dissimilar Species of Lake Victoria Cichlid Fish

We examined genetic structure among five species of Lake Victoria haplochromine cichlids in four island communities, using a full factorial sampling design that compared genetic differentiation between pairs of species and populations of varying morphological similarity and geographical proximity. We found that allopatric conspecific populations were on average significantly more strongly differentiated than sympatric heterospecific populations of morphologically similar species. Allopatric heterospecific populations of morphologically dissimilar species were most differentiated. Our work demonstrates that phenotypic divergence can be maintained and perhaps even evolve in sympatry despite considerable gene flow between species. Conversely, phenotypic resemblance among conspecific populations can be maintained despite geographical isolation. Additionally we show that anthropogenically increased hybridization does not affect all sympatric species evenly but predominantly affects morphologically similar and closely related species. This has important implications for the evolution of reproductive isolation between species These findings are also consistent with the hypothesis of speciation reversal due to weakening of divergent selection and reproductive isolation as a consequence of habitat homogenization and offers an evolutionary mechanistic explanation for the observation that species poor assemblages in turbid areas of the lake are characterized by just one or two species in each of a few morphologically distinct genera.

Gene flow and the maintenance of species boundaries

Hybrid zones are regions where individuals from genetically differentiated populations meet and mate, resulting in at least some offspring of mixed ancestry. Patterns of gene flow (introgression) in hybrid zones vary across the genome, allowing assessment of the role of individual genes or genome regions in reproductive isolation. Here, we document patterns of introgression between two recently diverged species of field crickets. We sampled at a very fine spatial scale and genotyped crickets for 110 highly differentiated single nucleotide polymorphisms (SNPs) identified through transcriptome scans. Using both genomic and geographic cline analysis, we document remarkably abrupt transitions (<100 m) in allele frequencies for 50 loci, despite high levels of gene flow at other loci. These are among the steepest clines documented for any hybridizing taxa. Furthermore, the cricket hybrid zone provides one of the clearest examples of the semi-permeability of species boundaries. Comparisons between data from the fine-scale transect and data (for the same set of markers) from sampling a much larger area in a different region of the cricket hybrid zone reveal consistent patterns of introgression for individual loci. The consistency in patterns of introgression between these two distant and distinct regions of the hybrid zone suggests that strong selection is acting to maintain abrupt discontinuities within the hybrid zone and that genomic regions with restricted introgression likely include genes that contribute to nonecological prezygotic barriers.

Effects of Interspecific Gene Flow on the Phenotypic Variance-Covariance Matrix in Lake Victoria Cichlids

Quantitative genetics theory predicts adaptive evolution to be constrained along evolutionary lines of least resistance. In theory, hybridization and subsequent interspecific gene flow may however rapidly change the evolutionary constraints of a population and eventually change its evolutionary potential, but empirical evidence is still scarce. Using closely related species pairs of Lake Victoria cichlids sampled from four different islands with different levels of interspecific gene flow, we tested for potential effects of introgressive hybridization on phenotypic evolution in wild populations. We found that these effects differed among our study species. Constraints measured as the eccentricity of phenotypic variance-covariance matrices declined significantly with increasing gene flow in the less abundant species for matrices that have a diverged line of least resistance. In contrast we find no such decline for the more abundant species. Overall our results suggest that hybridization can change the underlying phenotypic variance-covariance matrix, potentially increasing the adaptive potential of such populations.

Differences in male coloration are predicted by divergent sexual selection between populations of a cichlid fish

Female mating preferences can influence both intraspecific sexual selection and interspecific reproductive isolation, and have therefore been proposed to play a central role in speciation. Here, we investigate experimentally in the African cichlid fish Pundamilia nyererei if differences in male coloration between three para-allopatric populations (i.e. island populations with gene flow) of P. nyererei are predicted by differences in sexual selection by female mate choice between populations. Second, we investigate if female mating preferences are based on the same components of male coloration and go in the same direction when females choose among males of their own population, their own and other conspecific populations and a closely related para-allopatric sister-species, P. igneopinnis. Mate-choice experiments revealed that females of the three populations mated species-assortatively, that populations varied in their extent of population-assortative mating and that females chose among males of their own population based on different male colours. Females of different populations exerted directional intrapopulation sexual selection on different male colours, and these differences corresponded in two of the populations to the observed differences in male coloration between the populations. Our results suggest that differences in male coloration between populations of P. nyererei can be explained by divergent sexual selection and that population-assortative mating may directly result from intrapopulation sexual selection.