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Human-caused habitat fragmentation can drive rapid divergence of male genitalia.

ABSTRACT: The aim of this study rests on three premises: (i) humans are altering ecosystems worldwide, (ii) environmental variation often influences the strength and nature of sexual selection, and (iii) sexual selection is largely responsible for rapid and divergent evolution of male genitalia. While each of these assertions has strong empirical support, no study has yet investigated their logical conclusion that human impacts on the environment might commonly drive rapid diversification of male genital morphology. We tested whether anthropogenic habitat fragmentation has resulted in rapid changes in the size, allometry, shape, and meristics of male genitalia in three native species of livebearing fishes (genus: Gambusia) inhabiting tidal creeks across six Bahamian islands. We found that genital shape and allometry consistently and repeatedly diverged in fragmented systems across all species and islands. Using a model selection framework, we identified three ecological consequences of fragmentation that apparently underlie observed morphological patterns: decreased predatory fish density, increased conspecific density, and reduced salinity. Our results demonstrate that human modifications to the environment can drive rapid and predictable divergence in male genitalia. Given the ubiquity of anthropogenic impacts on the environment, future research should evaluate the generality of our findings and potential consequences for reproductive isolation.

SUBMITTER: Heinen-Kay JL

PROVIDER: S-EPMC4275096 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:South America's western coastline, extending in a near-straight line across some 35 latitudinal degrees, presents an elegant setting for assessing both contemporary and historic influences on cladogenesis in the marine environment. Southern bull-kelp (Durvillaea antarctica) has a broad distribution along much of the Chilean coast. This species represents an ideal model taxon for studies of coastal marine connectivity and of palaeoclimatic effects, as it grows only on exposed rocky coasts and is absent from beaches and ice-affected shores. We expected that, along the central Chilean coast, D. antarctica would show considerable phylogeographic structure as a consequence of the isolating effects of distance and habitat discontinuities. In contrast, we hypothesised that further south--throughout the region affected by the Patagonian Ice Sheet at the Last Glacial Maximum (LGM)--D. antarctica would show relatively little genetic structure, reflecting postglacial recolonisation. RESULTS:Mitochondrial (COI) and chloroplast (rbcL) DNA analyses of D. antarctica from 24 Chilean localities (164 individuals) revealed two deeply divergent (4.5 - 6.1% for COI, 1.4% for rbcL) clades from the centre and south of the country, with contrasting levels and patterns of genetic structure. Among populations from central Chile (32 degrees-44 degrees S), substantial phylogeographic structure was evident across small spatial scales, and a significant isolation-by-distance effect was observed. Genetic disjunctions in this region appear to correspond to the presence of long beaches. In contrast to the genetic structure found among central Chilean populations, samples from the southern Chilean Patagonian region (49 degrees-56 degrees S) were genetically homogeneous and identical to a haplotype recently found throughout the subantarctic region. CONCLUSIONS:Southern (Patagonian) Chile has been recolonised by D. antarctica relatively recently, probably since the LGM. The inferred trans-oceanic ancestry of these Patagonian populations supports the notion that D. antarctica is capable of long-distance dispersal via rafting. In contrast, further north in central Chile, the correspondence of genetic disjunctions in D. antarctica with long beaches indicates that habitat discontinuity drives genetic isolation among established kelp populations. We conclude that rafting facilitates colonisation of unoccupied shores, but has limited potential to enhance gene-flow among established populations. Broadly, this study demonstrates that some taxa may be considered to have either high or low dispersal potential across different temporal and geographic scales.

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Human-caused habitat fragmentation can drive rapid divergence of male genitalia.

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