How populations differentiate despite gene flow: sexual and natural selection drive phenotypic divergence within a land fish, the Pacific leaping blenny

Abstract

Background: Divergence between populations in reproductively important features is often vital for speciation. Many studies attempt to identify the cause of population differentiation in phenotype through the study of a specific selection pressure. Holistic studies that consider the interaction of several contrasting forms of selection are more rare. Most studies also fail to consider the history of connectivity among populations and the potential for genetic drift or gene flow to facilitate or limit phenotypic divergence. We examined the interacting effects of natural selection, sexual selection and the history of connectivity on phenotypic differentiation among five populations of the Pacific leaping blenny (Alticus arnoldorum), a land fish endemic to the island of Guam.

Results: We found key differences among populations in two male ornaments--the size of a prominent head crest and conspicuousness of a coloured dorsal fin--that reflected a trade-off between the intensity of sexual selection (male biased sex ratios) and natural selection (exposure to predators). This differentiation in ornamentation has occurred despite evidence suggesting extensive gene flow among populations, which implies that the change in ornament expression has been recent (and potentially plastic).

Conclusions: Our study provides an early snapshot of divergence in reproductively important features that, regardless of whether it reflects genetic or plastic changes in phenotype, could ultimately form a reproductive barrier among populations.

Figure 1

The Pacific leaping blenny (A. arnoldorum ) is a marine fish that spends its entire adult life on land. Adult males have a prominent head crest (A), which is absent in females. Five populations (B) at various distances from one another were studied around the island of Guam.

Figure 2

The allometry of ornamentation in the Pacific leaping blenny. Shown are natural-log data for the head crest, dorsal fin and ventral fin as a function of body length. The regression lines are the linear analogue of the allometric power function in which the allometric elevation corresponds to the intercept value, while the allometric exponent is represented by the regression slope (i.e., larger exponents result in steeper slopes and show the degree larger males invest disproportionally more in exaggerated ornamentation compared to smaller males). In order to properly estimate the allometric equation, all characteristics must be on the same scale. Crest and fin areas were therefore converted to a linear scale to match that of body length through a square-root transformation before then being natural-logged.

Figure 3

Population variation in phenotype. Shown is (A) adult body size, (B) the allometric parameters of the male head crest, and (C) the intensity of red of the dorsal fin (Δ^R/_G) as a function of predation (strikes to blenny models) and sex ratio. Grey, open circles are data points for individual fish, while black filled (male) and white filled (female) symbols are population means or allometric coefficients computed from RMA regressions reported in Table 2. Error bars correspond to 95% confidence intervals. Insets are predicted trends assuming predation selects against conspicuous characteristics, while sexual selection increases the conspicuousness of characteristics. For males, competition for mates was expected to increase with male biased sex ratios. For females, competition for mates was expected to decrease with male biased sex ratios. Solid trend lines are inclusive of all populations. Dashed trend lines exclude Talofofo (a population with an unusually red dorsal fin; C). Trend lines were computed based on parameter estimates from the best-supported models in Table 4 (those with ∆AIC ≤ 2.0).