Sympatric speciation as a consequence of male pregnancy in seahorses

Abstract

The phenomenon of male pregnancy in the family Syngnathidae (seahorses, pipefishes, and sea dragons) undeniably has sculpted the course of behavioral evolution in these fishes. Here we explore another potentially important but previously unrecognized consequence of male pregnancy: a predisposition for sympatric speciation. We present microsatellite data on genetic parentage that show that seahorses mate size-assortatively in nature. We then develop a quantitative genetic model based on these empirical findings to demonstrate that sympatric speciation indeed can occur under this mating regime in response to weak disruptive selection on body size. We also evaluate phylogenetic evidence bearing on sympatric speciation by asking whether tiny seahorse species are sister taxa to large sympatric relatives. Overall, our results indicate that sympatric speciation is a plausible mechanism for the diversification of seahorses, and that assortative mating (in this case as a result of male parental care) may warrant broader attention in the speciation process for some other taxonomic groups as well.ince the modern synthesis of evolutionary biology, the prevailing belief has been that most speciation events occur as a consequence of geographic barriers to gene flow (1, 2). However, in recent years a growing body of theoretical studies has established that sympatric speciation is possible and may be more common than thought previously (3-8). Nevertheless, there still exists a dearth of empirical systems in which sympatric speciation seems a likely explanatory mechanism (reviewed in ref. 8). The most convincing examples of sympatric speciation involve host-race formation by species such as Rhagoletis flies (9, 10) or pea aphids (8, 11) and ecological speciation in closed environments by taxa such as sticklebacks (12) or cichlids (13). Speciation in these types of systems probably involves the simultaneous evolution of assortative mating and phenotypic divergence through disruptive selection. Recent theoretical models show that such complex scenarios are plausible under biologically realistic conditions (5, 6, 14-16).The simplest situation favoring sympatric divergence occurs when both assortative mating and disruptive selection operate on the same phenotypic character (3,(17)(18)(19). Thus, if assortative mating appears in a population, even for reasons entirely unrelated to the speciation process, a lineage may in principle become predisposed to speciate whenever appropriate selective conditions arise. This model seems particularly feasible when mate choice involves ecologically important traits, which are likely to be the targets of selection, such as body size or habitat preference (3). This simplest scenario of sympatric speciation has not been empirically documented yet. Here we investigate the possibility that such a situation may have been important in the diversification of seahorses.This line of research was inspired by empirical field observations suggesting that seahorses mate assortatively by body size (20). Such ma...

Serial monogamy in the European long-snouted seahorse Hippocampus guttulatus

“…All wild broods tested were consistent with production from a single female-male mating, providing no evidence of departure from short-term (within a brood cycle) genetic monogamy in H. guttulatus, consistent with the breeding system previously observed for other seahorse species (Jones et al 1998(Jones et al , 2003Wilson and Martin-Smith 2007). Although H. guttulatus occurs at higher densities than most other seahorse species (Foster and Vincent 2004), it has been observed to be socially polygamous (Naud et al 2009) and may have skewed sex ratios in some populations (Woodall 2009): none of these factors appear to result in deviation from a genetically monogamous breeding system.…”

“…To date the mating strategies of just two species of seahorse, both native to Australia, have been genetically assessed. H. subelongatus was genetically monogamous within a brood cycle (Jones et al 1998) and males were faithful to a single female over two successive broods (Jones et al 2003), although low frequency of polygamy in successive broods has also been observed (Kvarnemo et al 2000). H. abdominalis was also found to be genetically monogamous in both low density wild populations and high density captive populations, despite the observation of social polygamy in wild populations (Wilson and Martin-Smith 2007).…”

Assortative Mating in Drosophila Adapted to a Microsite Ecological Gradient

“…Biologists once considered geographical isolation a necessary condition for evolution of sexual isolation, whereas sympatric speciation was viewed as much less plausible compared to geographic (allopatric) speciation (Mayr, 1963). Field studies, laboratory experiments, developments in population genetics theory, and phylogenetic and biogeographic data have all recently combined to shed a more favorable light on the process of sympatric speciation as a viable hypothesis (Bush, 1994;Dieckmann and Doebeli, 1999;Doebeli and Dieckmann 2003;Higashi et al, 1999;Jones et al, 2003;Kondrashov and Kondrashov 1999;Korol et al, 2000;Rice and Hostert, 1993;Smith, 1962;Turelli et al, 2001;Via, 2001). Several theoretical models have been proposed for evolution of premating isolation, including divergent ecological selection and sexual selection (Arnquist et al, 2000;Boughman, 2001;Higashi et al, 1999;Jiggins et al, 2001;Kondrashov and Kondrashov, 1999;Panhuis et al, 2001;Rundle et al, 2000;Turelli et al, 2001;Via 2001).…”

Reconstructing a radiation: the chiton genus Mopalia in the north Pacific

“…Briggs (2006) has advocated at least some role for sympatric speciation as a common mode of speciation within highly diverse areas such as the north Pacific and has further argued that such speciation can be much (perhaps 20 times) faster than allopatric speciation, with natural selection involved in the earliest stages of reproductive isolation. Examples of such speciation include Hellberg and Vacquier (1999), Hendry et al (2000), Dawson et al (2002) and Jones et al (2003). However Meyer's (2003) comprehensive work on cowries suggests that vicariant speciation in allopatry is the most common mechanism for divergence among Indo-West Pacific cypraeid gastropods.…”