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.

Evolution of affiliation: patterns of convergence from genomes to behaviour.

Affiliative behaviours have evolved many times across animals. Research on the mechanisms underlying affiliative behaviour demonstrates remarkable convergence across species spanning wide evolutionary distances. Shared mechanisms have been identified with genomic approaches analysing genetic variants and gene expression differences as well as neuroendocrine and molecular approaches exploring the role of hormones and signalling molecules. We review the genomic and neural basis of pair bonding and parental care across diverse taxa to shed light on mechanistic patterns that underpin the convergent evolution of affiliative behaviour. We emphasize that mechanisms underlying convergence in complex phenotypes like affiliation should be evaluated on a continuum, where signatures of convergence may vary across levels of biological organization. In particular, additional comparative studies within and across major vertebrate lineages will be essential in resolving when and why shared neural substrates are repeatedly targeted in the independent evolution of affiliation, and how similar mechanisms are evolutionarily tuned to give rise to species-specific variations in behaviour. This article is part of the theme issue 'Convergent evolution in the genomics era: new insights and directions'.

Diurnal foraging of a wild coral-reef fish Parapercis australis in relation to late-summer temperatures.

In situ observations of diurnal foraging behaviour of a common site-attached shallow reef mesopredator Parapercis australis during late summer, revealed that although diet composition was unaffected by seawater temperature (range 28.3-32.4°C), feeding strikes and distance moved increased with temperature up to 30.5°C, beyond which they sharply declined, indicative of currently living beyond their thermal optimum. Diel feeding strikes and distance moved were however, tightly linked to ambient temperature as it related to the population's apparent thermal optimum, peaking at times when it was approached (1230 and 1700 h) and declining up to four fold at times deviating from this. These findings suggest that although this population may be currently living beyond its thermal optimum, it copes by down regulating energetically costly foraging movement and consumption and under future oceanic temperatures, these behavioural modifications are probably insufficient to avoid deleterious effects on population viability without the aid of long-term acclimation or adaptation.

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.