The Dynamics of Male Brooding, Mating Patterns, and Sex Roles in Pipefishes and Seahorses (Family Syngnathidae)

Abstract

Abstract. Modern theory predicts that relative parental investment of the sexes in their young is a key factor responsible for sexual selection. Seahorses and pipefishes (family Syngnathidae) are extraordinary among fishes in their remarkable adaptations for paternal care and frequent occurrences of sex-role reversals (i.e., female-female competition for mates), offering exceptional opportunities to test predictions of sexual selection theory. During mating, the female transfers eggs into or onto specialized egg-brooding structures that are located on either the male's abdomen or its tail, where they are osmoregulated, aerated, and nourished by specially adapted structures. All syngnathid males exhibit this form of parental care but the brooding structures vary, ranging from the simple ventral gluing areas of some pipefishes to the completely enclosed pouches found in seahorses. We present a molecular phylogeny that indicates that the diversification of pouch types is positively correlated with the major evolutionary radiation of the group, suggesting that this extreme development and diversification of paternal care may have been an important evolutionary innovation of the Syngnathidae. Based on recent studies that show that the complexity of brooding structures reflects the degree of paternal investment in several syngnathid species, we predicted sex-role reversals to be more common among species with more complex brooding structures. In contrast to this prediction, however, both parsimony-and likelihoodbased reconstructions of the evolution of sex-role reversal in pipefishes and seahorses suggest multiple shifts in sex roles in the group, independent from the degree of brood pouch development. At the same time, our data demonstrate that sex-role reversal is positively associated with polygamous mating patterns, whereas most nonreversed species mate monogamously, suggesting that selection for polygamy or monogamy in pipefishes and seahorses may strongly influence sex roles in the wild. In the vast majority of animals, the male's sole contribution to his offspring is his sperm (Trivers 1972). As a result, even when the observed sex ratio of males to females is equal, the operational sex ratio is often biased toward males and males almost universally compete more strongly for mates, while females typically exert greater mate choice (Darwin 1871;Emlen and Oring 1977). Although most egg-laying fishes leave their eggs unprotected after spawning, sole male care is the predominant pattern in those species that care for their young (Blumer 1982). Paternal care is likely to increase offspring fitness, but may reduce the father's ability to invest in other offspring (i.e., a parental investment sensu Trivers 1972).Sex roles are defined by mating competition (Emlen and Oring 1977). Sex-role reversal occurs when females primarily compete for access to mates, as compared to conventional sex roles with male-male mating competition (cf. mating roles, Gwynne 1991). Traditionally, the concept of parental investment has been us...

An adaptive explanation for the horse-like shape of seahorses

“…As being able to strike from more distantly will increase the volume of water in which prey are susceptible to capture, the amount of potential food intake increases. In this way, the bending of the trunk into a horse-like shape, which improves the capacity to move the mouth anteriorly during the strike, can be regarded as functionally equivalent to the elongation of the snout in course of the evolution, the latter of which can be observed in several syngnathid taxa 3,13 .…”

Brooding fathers, not siblings, take up nutrients from embryos

“…Yet, since we know that small amounts of amino acids can be transferred from the male to the developing embryos (as shown in two studies in which the males were radioactively labelled but not the embryos; Ripley & Foran 2009; C. Kvarnemo, K. B. Mobley, C. Partridge, A. G. Jones & I. Ahnesjö 2003Ahnesjö -2004, it is still possible that a brooding male uses the absorbed nutrients to support the remaining embryos at a later stage in the brood cycle.…”

“…The brood pouch has also been suggested to facilitate transfer of steroids and growth hormones to the embryos, but this function has yet to be fully investigated (Haresign & Shumway 1981;Azzarello 1991;Ripley & Foran 2006). Among syngnathids, the brooding structure is highly variable, from the simple attachment of embryos to the male's body to more complex placenta-like brood pouches and sacs (Vincent et al 1995;Wilson et al 2001Wilson et al , 2003Carcupino et al 2002;Ripley & Foran 2006, 2009Stö lting & Wilson 2007).…”

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

“…2002; Wilson et al. 2003). Brood pouch complexity ranges from a complete lack of pouch, in which the eggs are attached to the skin of the male's tail or abdomen, through partially enclosed pouches consisting of lateral pouch plates, to fully enclosed pouches formed by two skin folds that seal in the middle during brooding, and the sac‐like fully closed pouch of seahorses (Herald 1959; Dawson 1985; Wilson et al.…”