Quantitative measures of sexual selection reveal no evidence for sex-role reversal in a sea spider with prolonged paternal care

Abstract

Taxa in which males alone invest in postzygotic care of offspring are often considered good models for investigating the proffered relationships between sexual selection and mating systems. In the pycnogonid sea spider Pycnogonum stearnsi, males carry large egg masses on their bodies for several weeks, so this species is a plausible candidate for sex-role reversal (greater intensity of sexual selection on females than on males). Here, we couple a microsatellite-based assessment of the mating system in a natural population with formal quantitative measures of genetic fitness to investigate the direction of sexual selection in P. stearnsi. Both sexes proved to be highly polygamous and showed similar standardized variances in reproductive and mating successes. Moreover, the fertility (number of progeny) of males and females appeared to be equally and highly dependent on mate access, as shown by similar Bateman gradients for the two sexes. The absence of sex-role reversal in this population of P. stearnsi is probably attributable to the fact that males are not limited by brooding space but have evolved an ability to carry large numbers of progeny. Body length was not a good predictor of male mating or reproductive success, so the aim of future studies should be to determine what traits are the targets of sexual selection in this species.

Bateman gradients in a promiscuous mating system

“…Interestingly, the levels of I and Is found in our system reached those usually reported for males of sexually dimorphic species (Vanpé et al 2008), and thus suggest that both sexes have the opportunity to be strongly selected to increase their MS. Females had I and Is of 2.27 and 2.05, respectively, which is much higher than values previously reported for females of other promiscuous species where all I and Is were lower than 1 (e.g., Jones et al 2002;Schulte-Hostedde et al 2004;Jones 2009;Barreto and Avise 2010;Munroe and Koprowski 2011). Also, although males in our system had I and Is 24 % higher than females, this is less than the differences reported among sexes in other promiscuous systems.…”

Sexual selection and its evolutionary consequences in female animals

“…Approximately equal positive Bateman gradients occur in two species with male parental care, the frog Allobates fermoralis (Ursprung et al, ) and the sea spider Pycnogonum stearnsi (Barreto & Avise, ); in one species where sperm from multiple matings are inferred to be necessary to maximise fertilisation success, the Dalmatian wall lizard ( Podarcis melisellensis ; Huyghe et al, ); in two species with dominant and sneaker males, the bull‐headed scarab ( Onthophagus taurus ; McCullough, Buzatto & Simmons, ) and the brown trout ( Salmo trutta ; Serbezov et al, ); in two species where male gametic investment rivals that of females, the mega‐sperm fruit flies Drosophila bifurca and D. lummei (Bjork & Pitnick, ); in one species where sexual conflict over mating frequency has likely led to sophisticated cryptic female choice, the water strider Gerris gilletei (Gagnon, Duchesne & Turgeon, ); in two species with substantial male or mutual mate choice, the small‐mouth salamander ( Ambystoma texanum ; Gopurenko, Williams & DeWoody, ) and the eastern chipmunk ( Tamias striatus ; Bergeron et al, ); and in several birds for which the benefits of polyandry remain unknown but are suspected to be indirect (Woolfenden, Gibbs & Sealy, ; Fitze & Le Galliard, ; Gerlach et al, ; Collet et al, ). Additionally, equal but flat Bateman gradients have been reported twice in both sexes of the Eurasian blue tit ( Cyanistes caeruleus ; García‐Navas et al, ; Schlicht & Kempenaers, ), suggesting a relaxed role of sexual selection in both sexes.…”

“…In sea spiders, males brood eggs on modified ovigerous legs, and females may initiate courtship (Bain & Govedich, ). However, complete sex role reversal does not occur (Barreto & Avise, ), likely because females may facultatively care for eggs in the case that the fertilising father is removed (Bain & Govedich, ). Nevertheless, females of at least one sea spider species ( Propallene saengeri ) may fight aggressively and even lethally in competition for access to males (Bain & Govedich, ).…”

Sexual selection favours male parental care, when females can choose

“…In the great tinamou, for example, females mate and leave offspring with multiple males, and males care for these offspring alone despite low paternity [15,16]. In the tessellated darter, males will care for completely unrelated young in order to attract females [17], and in sea spiders only males carry the eggs, despite sexual selection on males favouring higher male mating rates [18]. Current theory fails to explain the many species in which male-only care is found in the presence of sexual selection on males.…”