Brain size evolution in pipefishes and seahorses: the role of feeding ecology, life history and sexual selection.

Brain size varies greatly at all taxonomic levels. Feeding ecology, life history and sexual selection have been proposed as key components in generating contemporary diversity in brain size across vertebrates. Analyses of brain size evolution have, however, been limited to lineages where males predominantly compete for mating and females choose mates. Here, we present the first original data set of brain sizes in pipefishes and seahorses (Syngnathidae) a group in which intense female mating competition occurs in many species. After controlling for the effect of shared ancestry and overall body size, brain size was positively correlated with relative snout length. Moreover, we found that females, on average, had 4.3% heavier brains than males and that polyandrous species demonstrated more pronounced (11.7%) female-biased brain size dimorphism. Our results suggest that adaptations for feeding on mobile prey items and sexual selection in females are important factors in brain size evolution of pipefishes and seahorses. Most importantly, our study supports the idea that sexual selection plays a major role in brain size evolution, regardless of on which sex sexual selection acts stronger.

Evidence of paternal nutrient provisioning to embryos in broad-nosed pipefish Syngnathus typhle.

In two experiments, radioactively labelled nutrients (either (3)H-labelled amino-acid mixture or (14)C-labelled glucose) were tube-fed to brooding male Syngnathus typhle. Both nutrients were taken up by the males and radioactivity generally increased in the brood pouch tissue with time. Furthermore, a low but significant increase of (3)H-labelled amino acids in embryos was found over the experimental interval (48 h), whereas in the (14)C-glucose experiment the radioactivity was taken up by the embryos but did not increase over the experimental time (320 min). Uptake of radioisotopes per embryo did not differ with embryo size. A higher uptake mg(-1) tissue of both (3)H-labelled amino acids and (14)C-labelled glucose was found in smaller embryos, possibly due to a higher relative metabolic rate or to a higher surface-area-to-volume ratio compared to larger embryos. Uptake in embryos was not influenced by male size, embryonic developmental advancement or position in the brood pouch. It is concluded that brooding males provide amino acids, and probably also glucose, to the developing embryos in the brood pouch.

The ovarian structure and mode of egg production in two polygamous pipefishes: a link to mating pattern.

In this study, the ovarian structure and mode of egg production were examined in two pipefishes, the broad-nosed pipefish Syngnathus typhle and the straight-nosed pipefish Nerophis ophidion, which show different types of polygamous mating patterns. Syngnathus typhle showed an ovary with one germinal ridge and asynchronous egg production, corresponding to previous findings in other polygamous Syngnathus pipefishes. In contrast, the ovary of N. ophidion had two germinal ridges and eggs were produced synchronously in groups, similar to what has been observed in monogamous syngnathids. The egg production of N. ophidion, however, is clearly distinguished from that of monogamous syngnathids by the additional egg production after an ovulation. It is suggested that the differences in female mating strategies result from the difference in egg production process and that this is related to the difference in mating pattern between these two polygamous species.

The relationship between female body size and egg size in pipefishes.

Comparing five species of pipefish, egg size was significantly larger in species with brood pouches (Syngnathus typhle, Syngnathus acus and Syngnathus rostellatus) than in species without brood pouches (Entelurus aequoreus and Nerophis ophidion). Egg size correlated positively with female body size in species with brood pouches, but was similar across female sizes in the species lacking pouches. These results may reflect differences in offspring competition as a consequence of variable offspring relatedness within a brood, due to the mating systems adopted by the different species and the presence or absence of a brood pouch.

Male pregnancy in seahorses and pipefishes (family Syngnathidae): rapid diversification of paternal brood pouch morphology inferred from a molecular phylogeny.

In contrast to the majority of vertebrate species, primary male parental care is common in fishes and encompasses a remarkable diversity of adaptations. Seahorses and pipefishes (Family Syngnathidae) exhibit some of the most specialized forms of paternal care in animals and so are ideally suited to the study of the evolution of male parental care. During mating, female syngnathids transfer eggs to specialized morphological structures that are located on either the abdomen or tail of the male. The male provides all postfertilization parental care and has morphological and physiological adaptations to osmoregulate, aerate, and even nourish the developing embryos. While all syngnathid species are adapted for paternal care, the brooding structure with which this is accomplished varies between species, from simple ventral gluing areas to much more complex structures such as the completely enclosed pouches of the seahorses. Our combined cytochrome b-, 12S rDNA-, and 16S rDNA-based molecular phylogeny of syngnathid fishes demonstrates that rapid diversification of male brooding structures has been associated with the major evolutionary radiation of the group, suggesting that development and diversification of structures involved in paternal care may have been key evolutionary innovations of the Syngnathidae. Molecular analyses also highlight geographical centers of biodiversity and suggest interoceanic migration of Syngnathus pipefishes from their center of origin in the Pacific.

Female fifteen-spined sticklebacks prefer better fathers.

We studied how male fifteen-spined sticklebacks, Spinachia spinachia, vary in paternal competence, whether males advertise their competence and whether females prefer better fathers. In this species the male alone provides care for the offspring through nest building, fanning, cleaning and protecting the eggs. We found no female preference for larger males. Instead, females preferred males that during the subsequent paternal phase fanned their nests in shorter fanning bouts. Such males enjoyed a significantly higher hatching success because they fanned more often than males with longer fanning bouts. Males that fanned for short bouts during the paternal phase were also able to increase their fin beat rate. Frequent fanning and high fin beat rates may improve the flow of oxygen to the eggs. Beat rate may be a condition-dependent trait, because males that lost more weight were unable to increase their fin beat rate. During courtship, males perform behaviours such as displacement fanning and body shaking. Females preferred males showing more frequent body shakes during courtship. Body shake frequency correlated positively with hatching success, and negatively with mean fanning bout duration during the paternal phase. The results indicate that female S. spinachia show a preference for direct benefits in terms of better paternal care, and that males may signal this ability to females by shaking their body during courtship. Copyright 1998 The Association for the Study of Animal Behaviour.

The dynamics of operational sex ratios and competition for mates.

In sexually reproducing animals, individuals of one sex may have to compete for access to mating partners of the opposite sex. The operational sex ratio (OSR) is central in predicting the intensity of mating competition and which sex is competing for which. Thanks to recent theoretical and empirical advances, particularly by exploring the concept of OSR, sexual selection studies today are becoming more fine-tuned and dynamic. The original role of parental investment in predicting sexual selection has recently been complemented by the use of sexual differences in potential reproductive rates (PRR).

Pipefishes and seahorses: Are they all sex role reversed?

The male pregnancy of pipefishes and seahorses has led to the inference that females compete most intensely for access to mates, because males limit female reproduction. However, recent work has shown that in different species either sex may be the predominant competitor for mates. In this family, there is an apparent association between the mating pattern and the sex roles: polygamous species show reversed sex roles whereas monogamous species exhibit 'conventional' sex roles. These studies emphasize that sex role reversal is not synonymous with male parental care.