Before the implications of our findings can be fully appreciated, we need to first interpret the absence of genetic differentiation among populations. While ecological barriers isolate adult populations, the Pacific leaping blenny has a roughly one month pelagic larval phase (Platt and Ord, unpublished data). During this larval phase, larvae have the capacity to disperse several hundred kilometers around the island (Cooke GM, Schlub TE, Sherwin WB, Ord TJ: Understanding the spatial scale of genetic connectivity at sea: insights from a land fish and a meta-analysis. In review). Given the distance between our furthest populations was less than a hundred kilometers and that pelagic larval dispersal is a well-known cause of high genetic connectivity among marine fish (e.g. [34–36]; including pelagic marine fish populations around Guam ), the lack of genetic differentiation among populations of Pacific leaping blenny almost certainly reflects contemporary gene flow rather than the recent isolation of populations (see Cooke et al. for discussion).
This high gene flow among populations is significant because the general assumption has been that populations only phenotypically diverge in the absence of the homogenizing effects of gene flow [23, 38]. This in turn predicts that features that might facilitate reproductive isolation are unlikely to evolve if members from different populations frequently mate with one another. This has generated considerable debate over the extent to which adaptive differentiation might occur in response to geographic gradients in selection (e.g., along habitat gradients) and the likelihood of sympatric speciation occurring in nature . Yet there are compelling examples of both adaptive differentiation among parapatric populations and speciation occurring without geographic isolation [40–44]. The question is whether these are special cases or whether adaptive differentiation is more common in the presence of gene flow than currently assumed.
Our results suggest that phenotypic divergence among populations of the Pacific leaping blenny has resulted from a complex interaction of natural and sexual selection, and in the presence of high gene flow among populations (as evidenced by the absence of genetic differentiation among populations). Sexual selection measured by male-biased sex ratios was clearly associated with population divergence in the exaggeration of the male head crest, and has also potentially increased the conspicuousness of the dorsal fin colouration in males and females. In contrast, natural selection operating through predation appears to have dampened the conspicuousness of dorsal fin colouration in at least males.
The strong, positive correlation between male head crest allometry and sex ratio reflects an increase in ornament size as population sex ratios became increasingly skewed towards males. This implies that greater competition for females has led to an increase in the investment made by large males in the size of the head crest (selection on the allometric exponent). Males defend rock holes from other males and attempt to entice females to enter and spawn in these holes through an elaborate head-nodding display. The head crest is clearly visible during this display and presumably an additional feature used by females to assess the quality of males. Yet this divergence among populations in ornament size has occurred in the presence of high gene flow. Presumably, a large adult male from Talofofo would have more difficulty in mating with females at Umatac or Pago because he would be competing with more males and males with larger head crests (e.g., Figure 2). The question that follows is the extent differences in head crest allometry (and the color of male dorsal fins) are genetic or plastic in origin. A high rate of larval dispersal among populations, as suggested by our genetic data, implies ornaments are plastic. Such plasticity would likely be dependent on a population sex ratio that is in itself temporally variable (sex ratio will tend to reflect the sex of larvae that happen to settle at a given location). All populations might therefore share the same underlying (evolutionary) allometry in head crest expression, but the observed investment in large head crests by large males (leading to an exaggerated allometric exponent in a population) depends on the level of competition for mates in a given population at a given point in time. That is, the density of males dictates the extent to which male larvae settling at that location subsequently invest in the exaggeration of the head crest. This is not to say that plasticity breaks the allometric constraint associated with ornament development (small males will still be limited in the overall size of their head crests compared to larger males), rather that the extent males “choose” to invest to reach their maximum potential ornament size varies by population. This type of plasticity has been demonstrated for other sexually selected characteristics (e.g., call rate in crickets: [45, 46]), but has generally not been considered in the context of the allometry of ornaments (but see ). If ornamentation is developmentally plastic, then ornament divergence among populations might still limit reproduction among adults from different populations, but genetic isolation would only occur if larval dispersal connecting populations was disrupted in some way. In this sense, plasticity in ornament expression has the potential to facilitate future reproductive isolation among populations if ocean currents or the nature of storm surges facilitating larval dispersal were to change around Guam (e.g., because of climate change). Future studies on the Pacific leaping blenny will need to assess the extent to which the size of the head crest is plastic and the implications of this for reproductive isolation among populations.
The population differences in the allometric exponent of head crest size, but not its allometric elevation, has other implications as well. Classically, evolutionary change in the allometric exponent of sexually selected features was believed to be constrained by the very developmental costs believed to produce the distinctive pattern of positive allometry in ornaments (see  and references cited therein). These costs should be less apparent in the allometric elevation of ornaments, which should subsequently be more evolutionary liable than the exponent [49, 50]. This has been confirmed by selection experiments (e.g., [31, 51]; see also studies reviewed by Bonduriansky ) and at least one phylogenetic comparative study that documented extremely slow evolutionary change in within-species exponents of sexually selected characteristics (which is consistent with the notion that the exponent is developmentally constrained in some way ).The findings of our study clearly differed from these past findings. The allometric exponent of a prominent ornament in the Pacific leaping blenny—the head crest—seemed to be highly reactive to changes in the intensity of sexual selection (specifically, sex ratio), whereas there was virtually no change in the allometric elevation of the ornament under the same conditions (Figure 3B). That is, plastic or genetic changes in allometric exponent in response to changes in sexual selection have not subsequently lead to an overall change in head crest size in a population (a change in head crest elevation): small males are still limited in their ability to produce larger head crests. This implies that allometric elevations are not plastic in the Pacific leaping blenny, and either the intensity of sexual selection has not been stable enough from generation to generation to induce adaptive change (e.g., sex ratios vary temporally) or that evolutionary change in allometric elevations are constrained in some way (which contradicts previous assumptions about the evolvability of the allometric elevation relative to the exponent).
Going beyond the study of ornament allometries, there have been few studies that have examined the potential trade-off between sexual selection and predation in the expression of ornaments and other sexual signals more generally. Of these studies, most have examined colour signals that are constantly exposed to both conspecifics and predators (e.g., body colouration and patterning; [9, 53]). However, when an animal’s colour signal can be concealed from predators—for example, by restricting the colour signal to a part of the body only exposed during a social display to conspecifics ; this study—the influence of predation should be reduced. In the Pacific leaping blenny, the dorsal fin was only erected and visible during bouts of signaling . In this sense, the impact of predation on the conspicuousness of the dorsal fin colouration should be low. Yet, our results suggested that the intensity of dorsal fin redness in males was potentially the target of predation (Figure 3C). In contrast, however, dorsal fin colouration was far more conspicuous in females (compare the range of ΔR/G values in Figure 3C), but female dorsal fin colour did not appear to be influenced by predation. We suspect this reflects differences in the frequency of dorsal fin displays between the sexes, which were much higher in males than females (males: roughly one fin display every 15 minutes; females: roughly one fin display every hour; computed from the data archive of ). More generally, though, our results imply that any conspicuous behavior, if used frequently enough, can be the target of predation that can lead to measureable differences in ornament expression among populations.
There are, of course, other potential selection pressures that were not examined by our study and may also have contributed to population divergences in ornamentation or body size. For example, ornaments are only effective sexual signals if mates and rivals are able to distinguish those ornaments from habitat backgrounds. This was an implicit assumption in our study and has been confirmed by previous study for at least the dorsal fin . Given that habitat backgrounds do tend to vary among locations , some of the variation in dorsal fin coloration could be attributed to selection for increased conspicuousness in local environments. Furthermore, red pigmentation in fish has often been shown to be carotenoid based and consequently diet dependent (e.g., ). Differences among populations in the availability of carontenoids in the environment are another source of potential variation that was not examined here. The availability of food resources more generally might also account for differences in body size among populations (Figure 3A).