Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy

Abstract

Male pregnancy in seahorses, pipefishes and sea dragons (family Syngnathidae) represents a striking reproductive adaptation that has shaped the evolution of behaviour and morphology in this group of fishes. In many syngnathid species, males brood their offspring in a specialized pouch, which presumably evolved to facilitate male parental care. However, an unexplored possibility is that brood pouch evolution was partly shaped by parent-offspring or sexual conflict, processes that would result in trade-offs between current and future pregnancies. Here we report a controlled breeding experiment using the sexually dimorphic Gulf pipefish, Syngnathus scovelli, to test for post-copulatory sexual selection within broods and for trade-offs between successive male pregnancies as functions of female attractiveness. Offspring survivorship within a pregnancy was affected by the size of a male's mate, the number of eggs transferred and the male's sexual responsiveness. Significantly, we also found that embryo survivorship in a current pregnancy was negatively related to survivorship in the prior pregnancy, clearly demonstrating fitness trade-offs between broods. Overall, our data indicate that post-copulatory sexual selection and sexual conflict occur in Gulf pipefishes. The conflict seems to be mediated by a strategy of cryptic choice in which males increase rates of offspring abortion in pregnancies from unattractive mothers to retain resources for future reproductive opportunities. Hence, the male brood pouch of syngnathid fishes, which nurtures offspring, also seems to have an important role as an arbiter of conflict between the sexes.

Evolutionary ecology of pipefish brooding structures: embryo survival and growth do not improve with a pouch

“…2010). Thus, the generally lower embryo survival found in the species with brood pouches indicates that pouches did not evolve primarily to improve offspring survival, but more likely as a response to other selective processes such as mate choice (Paczolt and Jones 2010) or family conflicts (Kamel et al. 2010).…”

“…Seadragons (genus Phyllopteryx or Phycodurus ) would have been such examples, but as they only occur in West and Southern Australia under different ecological conditions, it was not tenable to include them in this study. Second, in addition to all the potential advantages brood pouches provide in terms of care (e.g., physical protection, nutrient provision, and osmoregulation) to the developing embryos, brood pouches may also enable males to have greater control over the number of embryos brooded and which embryos to support (Paczolt and Jones 2010; Sagebakken et al. 2010).…”

Absence of major histocompatibility complex class II mediated immunity in pipefish, Syngnathus typhle : evidence from deep transcriptome sequencing

“…As a sex-role reversed fish, the pipefish S. typhle, is a widely studied model species in evolutionary biology [7,8]. Females lay eggs into the male brood pouch, where they are fertilized and nourished [9].…”

Female pipefish can detect the immune status of their mates

“…A preference for MHCcompatible mates, associated with the lack of detectable visual cues associated with heat-killed Vibrio infection, may mask or override a preference for uninfected females in our experiment. Furthermore, because males are in control over egg development and can actively abort and absorb eggs of unattractive females (Paczolt and Jones 2010;Sagebakken et al 2010), post-copulatory processes can correct male mate decisions. Therefore, mate preference patterns identified here may not reflect the whole complexity of mate choice behavior.…”