Gene expression correlates of social evolution in coral reef butterflyfishes.

Animals display remarkable variation in social behaviour. However, outside of rodents, little is known about the neural mechanisms of social variation, and whether they are shared across species and sexes, limiting our understanding of how sociality evolves. Using coral reef butterflyfishes, we examined gene expression correlates of social variation (i.e. pair bonding versus solitary living) within and between species and sexes. In several brain regions, we quantified gene expression of receptors important for social variation in mammals: oxytocin (OTR), arginine vasopressin (V1aR), dopamine (D1R, D2R) and mu-opioid (MOR). We found that social variation across individuals of the oval butterflyfish, Chaetodon lunulatus, is linked to differences in OTR,V1aR, D1R, D2R and MOR gene expression within several forebrain regions in a sexually dimorphic manner. However, this contrasted with social variation among six species representing a single evolutionary transition from pair-bonded to solitary living. Here, OTR expression within the supracommissural part of the ventral telencephalon was higher in pair-bonded than solitary species, specifically in males. These results contribute to the emerging idea that nonapeptide, dopamine and opioid signalling is a central theme to the evolution of sociality across individuals, although the precise mechanism may be flexible across sexes and species.

Variation in social systems within Chaetodon butterflyfishes, with special reference to pair bonding.

For many animals, affiliative relationships such as pair bonds form the foundation of society and are highly adaptive. Animal systems amenable for comparatively studying pair bonding are important for identifying underlying biological mechanisms, but mostly exist in mammals. Better establishing fish systems will enable comparison of pair bonding mechanisms across taxonomically distant lineages that may reveal general underlying mechanistic principles. We examined the utility of wild butterflyfishes (f: Chaetodontidae; g: Chaetodon) for comparatively studying pair bonding. Using stochastic character mapping, we provide the first analysis of the evolutionary history of butterflyfish sociality, revealing that pairing is ancestral, with at least seven independent transitions to gregarious grouping and solitary behavior since the late Miocene. We then formally verified social systems in six sympatric and wide-spread species representing a clade with one ancestrally reconstructed transition from paired to solitary grouping at Lizard Island, Australia. In situ observations of the size, selective affiliation and aggression, fidelity, and sex composition of social groups confirmed that Chaetodon baronessa, C. lunulatus, and C. vagabundus are predominantly pair bonding, whereas C. rainfordi, C. plebeius, and C. trifascialis are predominantly solitary. Even in the predominantly pair bonding species, C. lunulatus, a proportion of adults (15%) are solitary. Importantly, inter- and intra-specific differences in social systems do not co-vary with other previously established attributes, including parental care. Hence, the proposed butterflyfish populations are promising for inter- and intra-species comparative analyses of pair bonding and its mechanistic underpinnings. Avenues for further developing the system are proposed, including determining whether the aforementioned utility of these species applies across their geographic disruptions.

Pair bond endurance promotes cooperative food defense and inhibits conflict in coral reef butterflyfish.

Pair bonding is generally linked to monogamous mating systems, where the reproductive benefits of extended mate guarding and/or of bi-parental care are considered key adaptive functions. However, in some species, including coral reef butterflyfishes (f. Chaetodonitidae), pair bonding occurs in sexually immature and homosexual partners, and in the absence of parental care, suggesting there must be non-reproductive adaptive benefits of pair bonding. Here, we examined whether pair bonding butterflyfishes cooperate in defense of food, conferring direct benefits to one or both partners. We found that pairs of Chaetodon lunulatus and C. baronessa use contrasting cooperative strategies. In C. lunulatus, both partners mutually defend their territory, while in C. baronessa, males prioritize territory defence; conferring improvements in feeding and energy reserves in both sexes relative to solitary counterparts. We further demonstrate that partner fidelity contributes to this function by showing that re-pairing invokes intra-pair conflict and inhibits cooperatively-derived feeding benefits, and that partner endurance is required for these costs to abate. Overall, our results suggest that in butterflyfishes, pair bonding enhances cooperative defense of prey resources, ultimately benefiting both partners by improving food resource acquisition and energy reserves.

Aggressive females become aggressive males in a sex-changing reef fish.

Many animal populations display consistent individual differences in suites of correlated behaviours. While these so called 'animal personalities' can substantially influence the ecology and evolution of populations, little is known about cross-sex correlations of behaviour and thus the potential of personality to limit sex-specific behavioural adaptations. Here, we experimentally induced sex-change in the sequentially hermaphroditic reef fish Parapercis cylindrica and demonstrate the existence of tight cross-sex correlations for two behaviours with presumed different sex-specific optima. Individuals that were relatively more active and aggressive females were found to become relatively more active and aggressive males. By identifying personality as a potential genetic constraint on the resolution of intralocus sexual conflict over behaviour, our findings have important ecological and evolutionary implications for a wide range of species.

Density-dependent sex ratio adjustment and the allee effect: a model and a test using a sex-changing fish.

Positive density dependence (i.e., the Allee effect; AE) often has important implications for the dynamics and conservation of populations. Here, we show that density-dependent sex ratio adjustment in response to sexual selection may be a common AE mechanism. Specifically, using an analytical model we show that an AE is expected whenever one sex is more fecund than the other and sex ratio bias toward the less fecund sex increases with density. We illustrate the robustness of this pattern, using Monte Carlo simulations, against a range of body size-fecundity relationships and sex-allocation strategies. Finally, we test the model using the sex-changing polygynous reef fish Parapercis cylindrica; positive density dependence in the strength of sexual selection for male size is evidenced as the causal mechanism driving local sex ratio adjustment, hence the AE. Model application may extend to invertebrates, reptiles, birds, and mammals, in addition to over 70 reef fishes. We suggest that protected areas may often outperform harvest quotas as a conservation tool since the latter promotes population fragmentation, reduced polygyny, a balancing of the sex ratio, and hence up to a 50% decline in per capita fecundity, while the former maximizes polygyny and source-sink potential.

Differing mechanisms underlie sexual size-dimorphism in two populations of a sex-changing fish.

Variability in the density of groups within a patchy environment lead to differences in interaction rates, growth dynamics and social organization. In protogynous hermaphrodites there are hypothesised trade-offs among sex-specific growth, reproductive output and mortality. When differences in density lead to changes to social organization the link between growth and the timing of sex-change is predicted to change. The present study explores this prediction by comparing the social organisation and sex-specific growth of two populations of a protogynous tropical wrasse, Halichoeres miniatus, which differ in density. At a low density population a strict harem structure was found, where males maintained a tight monopoly of access and spawning rights to females. In contrast, at a high density population a loosely organised system prevailed, where females could move throughout multiple male territories. Otolith microstructure revealed the species to be annual and deposit an otolith check associated with sex-change. Growth trajectories suggested that individuals that later became males in both populations underwent a growth acceleration at sex-change. Moreover, in the high density population, individuals that later became males were those individuals that had the largest otolith size at hatching and consistently deposited larger increments throughout early larval, juvenile and female life. This study demonstrates that previous growth history and growth rate changes associated with sex change can be responsible for the sexual dimorphism typically found in sex-changing species, and that the relative importance of these may be socially constrained.

Sexual selection explains sex-specific growth plasticity and positive allometry for sexual size dimorphism in a reef fish.

In 1950, Rensch noted that in clades where males are the larger sex, sexual size dimorphism (SSD) tends to be more pronounced in larger species. This fundamental allometric relationship is now known as 'Rensch's rule'. While most researchers attribute Rensch's rule to sexual selection for male size, experimental evidence is lacking. Here, we suggest that ultimate hypotheses for Rensch's rule should also apply to groups of individuals and that individual trait plasticity can be used to test those hypotheses experimentally. Specifically, we show that in the sex-changing fish Parapercis cylindrica, larger males have larger harems with larger females, and that SSD increases with harem size. Thus, sexual selection for male body size is the ultimate cause of sexual size allometry. In addition, we experimentally illustrate a positive relationship between polygyny potential and individual growth rate during sex change from female to male. Thus, sexual selection is the ultimate cause of variation in growth rate, and variation in growth rate is the proximate cause of sexual size allometry. Taken together, our results provide compelling evidence in support of the sexual selection hypothesis for Rensch's rule and highlight the potential importance of individual growth modification in the shaping of morphological patterns in Nature.

Fish ears are sensitive to sex change.

Many reef fishes change sex during their life. The testing of life-history theory and effective fisheries management therefore relies on our ability to detect when this fundamental transition occurs. This study experimentally illustrates the potential to glean such information from the otolithic bodies of the inner-ear apparatus in the sex-changing fish Parapercis cylindrica. It will now be possible to reconstruct the complete, often complex life history of hermaphroditic individuals from hatching through to terminal reproductive status. The validation of sex-change associated otolith growth also illustrates the potential for sex-specific sensory displacement. It is possible that sex-changing fishes alter otolith composition, and thus sensory-range specificity, to optimize life history in accordance with their new reproductive mode.