Abstract

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.

Highlights

  • Social bonds are foundational to many animal societies [1, 2]

  • This resulted in a posterior distribution of dated trees, which were summarized as a maximum clade credibility tree (MCC)

  • Pair bonding is the most likely ancestral social system of the family based on the 10,000 stochastic character mappings summarized on an MCC tree (Fig 2)

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Summary

Introduction

Social bonds are foundational to many animal societies [1, 2]. Arguably, the most extreme form of social bond is the pair bond—a selective, relatively pro-social and enduring affiliation between two individuals that is maintained beyond (or outside of) reproduction. A scarcity of complementary research among other organisms has led to little being known about the evolution pair bonding mechanisms across vertebrates, making it difficult to identify general principles for the sub-phylum. In many current mammal and avian systems for comparatively studying pair bonding, variation in pair bonding is confounded with variation in other life-history attributes, making it difficult to identify causal mechanisms for pair bonding. This problem is perhaps most severe for male mammalian model species, wherein pair bonding species are parental and non-pair bonding species are non-parental, resulting in little being known about the mechanisms of pair bonding independently from parental care in this sex. Expanding pair bonding systems to better include teleost fishes is a promising solution to these limitations, owing to their distant taxonomic relation to mammalian and avian systems [27], unparalleled species diversity [28], and extreme diversity in social systems, ecology, and behaviour [29, 30]

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