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Drivers of Sociality in Gobiodon Fishes: an Assessment of Phylogeny, Ecology and Life-History Martin Hing University of Wollongong, [email protected]

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Drivers of Sociality in Gobiodon Fishes: an Assessment of Phylogeny, Ecology and Life-History Martin Hing University of Wollongong, Mlh913@Uowmail.Edu.Au View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Research Online University of Wollongong Research Online Faculty of Science, Medicine and Health - Papers: Faculty of Science, Medicine and Health Part B 2019 Drivers of sociality in Gobiodon fishes: An assessment of phylogeny, ecology and life-history Martin Hing University of Wollongong, [email protected] Oya S. Klanten University of Technology Sydney, [email protected] Marian Y. L Wong University of Wollongong, [email protected] Mark P. Dowton University of Wollongong, [email protected] Publication Details Hing, M. L., Klanten, O. Selma., Wong, M. Y.L. & Dowton, M. (2019). Drivers of sociality in Gobiodon fishes: An assessment of phylogeny, ecology and life-history. Molecular Phylogenetics and Evolution, 137 263-273. Research Online is the open access institutional repository for the University of Wollongong. For further information contact the UOW Library: [email protected] Drivers of sociality in Gobiodon fishes: An assessment of phylogeny, ecology and life-history Abstract What drives the evolution of sociality in animals? Many robust studies in terrestrial organisms have pointed toward various kinship-based, ecological and life-history traits or phylogenetic constraint which have played a role in the evolution of sociality. These traits are not mutually exclusive and the exact combination of traits is likely taxon-specific. Phylogenetic comparative analyses have been instrumental in identifying social lineages and comparing various traits with non-social lineages to give broad evolutionary perspectives on the development of sociality. Few studies have attempted this approach in marine vertebrate systems. Social marine fishes are particularly interesting because many have a pelagic larval phase and non-conventional life- history strategies (e.g. bi-directional sex-change) not often observed in terrestrial animals. Such strategies provide novel insights into terrestrially-derived theories of social evolution. Here, we assess the strength of the phylogenetic signal of sociality in the Gobiodon genus with Pagel's lambda and Blomberg's K parameters. We found some evidence of a phylogenetic signal of sociality, but factors other than phylogenetic constraint also have a strong influence on the extant social state of each species. We then use phylogenetic generalized least squares analyses to examine several ecological and life-history traits that may have influenced the evolution of sociality in the genus. We found an interaction of habitat size and fish length was the strongest predictor of sociality. Sociality in larger species was more dependent on coral size than in smaller species, but smaller species were more social overall, regardless of coral size. Finally, we comment on findings regarding the validity of the species G. spilophthalmus which arose during the course of our research. These findings in a group of marine fishes add a unique perspective on the evolution of sociality to the excellent terrestrial work conducted in this field. Publication Details Hing, M. L., Klanten, O. Selma., Wong, M. Y.L. & Dowton, M. (2019). Drivers of sociality in Gobiodon fishes: An assessment of phylogeny, ecology and life-history. Molecular Phylogenetics and Evolution, 137 263-273. This journal article is available at Research Online: https://ro.uow.edu.au/smhpapers1/738 Drivers of sociality in Gobiodon fishes: An assessment of phylogeny, ecology and life-history Martin L. Hinga, O. Selma Klantenb, Marian Y.L. Wonga, Mark Dowtonc a Centre for Sustainable Ecosystems Solutions, School of Earth, Atmospheric and Life Sciences, University of Wollongong, Australia b Fish Ecology Laboratory, School of Life Sciences, University of Technology Sydney, Australia c Molecular Horizons, School of Chemistry and Molecular Bioscience, University of Wollongong, Australia * Corresponding author E-mail: [email protected] (MH) Highlights A phylogeny for the genus Gobiodon was inferred from seven molecular markers and resolved several previously unresolved nodes There is some evidence for a phylogenetic signal of sociality in the genus Gobiodon A combination of ecological and life-history factors best predicts sociality in the genus Gobiodon Phylogenetic analysis reveals potential issues surrounding the identification and validity of Gobiodon spilophthalmus Abstract What drives the evolution of sociality in animals? Many robust studies in terrestrial organisms have pointed toward various kinship-based, ecological and life-history traits or phylogenetic constraint which have played a role in the evolution of sociality. These traits are not mutually exclusive and the exact combination of traits is likely taxon-specific. Phylogenetic comparative analyses have been instrumental in identifying social lineages and comparing various traits with non-social lineages to give broad evolutionary perspectives on the development of sociality. Few studies have attempted this approach in marine vertebrate systems. Social marine fishes are particularly interesting because many have a pelagic larval phase and non-conventional life-history strategies (e.g. bi-directional sex- change) not often observed in terrestrial animals. Such strategies provide novel insights into terrestrially-derived theories of social evolution. Here, we assess the strength of the phylogenetic signal of sociality in the Gobiodon genus with Pagel’s lambda and Blomberg’s K parameters. We found some evidence of a phylogenetic signal of sociality, but factors other than phylogenetic constraint also have a strong influence on the extant social state of each species. We then use phylogenetic generalized least squares analyses to examine several ecological and life-history traits that may have influenced the evolution of sociality in the genus. We found an interaction of habitat size and fish length was the strongest predictor of sociality. Sociality in larger species was more dependent on coral size than in smaller species, but smaller species were more social overall, regardless of coral size. Finally, we comment on findings regarding the validity of the species G. spilophthalmus which arose during the course of our research. These findings in a group of marine fishes add a unique perspective on the evolution of sociality to the excellent terrestrial work conducted in this field. Keywords Gobiodon; Sociality; Phylogeny; Ecological factors; Life-history factors; Gobiodon spilophthalmus c.f. 1 1. Introduction 2 The question of how sociality first arose in animals has attracted much attention in the fields of 3 evolutionary ecology and animal behaviour. Many mechanisms are thought to contribute to the 4 evolution of sociality including ecological factors, life-history traits and phylogeny (Arnold and Owens, 5 1998; Emlen, 1982; Hamilton, 1964; Hatchwell and Komdeur, 2000; reviewed in Hing et al., 2017; Kokko 6 and Ekman, 2002). These features are not mutually exclusive and may be highly dependent on each 7 other (Arnold and Owens, 1998; Chapple, 2003). Hamilton’s rule predicts that sociality should evolve 8 under certain combinations of relatedness and costs and benefits of social actions and is widely 9 regarded as a universal framework to study social evolution (Bourke, 2014; Hamilton, 1964). Ecology, 10 life-history and relatedness change the costs and benefits conferred to individuals within the group. 11 Under this framework, individuals should receive greater inclusive fitness benefits if they form social 12 groups with close relatives (Briga et al., 2012; Hughes et al., 2008). Groups consisting of unrelated 13 individuals are also possible if ecological or life-history factors alter the direct costs and benefits of 14 group living such that the benefits outweigh the costs (e.g. Buston et al., 2007; Riehl, 2011). 15 Phylogenetic relationships among taxa can constrain the evolution of sociality which may predispose 16 species to sociality (e.g. Agnarsson, 2002; Nowicki et al., 2018; Schneider and Kappeler, 2014; 17 Smorkatcheva and Lukhtanov, 2014). However, the extant state of sociality may depend on various 18 ecological and life-history conditions (Chapple, 2003; Rubenstein and Lovette, 2007; Schürch et al., 19 2016). For example, altered environmental conditions and extreme weather events could reduce habitat 20 sizes for a normally social species, increasing animal density and increasing conflict within the group 21 ultimately leading to a reduction in sociality (Hing et al., 2018). On the other hand, some species in 22 which sociality has a strong phylogenetic signal (that is, sociality is highly constrained), may maintain 23 their sociality regardless of other factors (Kruckenhauser et al., 1999; Nowicki et al., 2018; Shultz et al., 24 2011). In either case, understanding the strength of the relationship between phylogeny and sociality 25 can help us to understand what role phylogeny played in the evolution of sociality. 26 The majority of studies of sociality have been conducted on birds, mammals and invertebrates wherein 27 subordinates are usually related to dominants and display natal philopatry (Bourke, 2011; Hing et al., 28 2017; Jennions and Macdonald, 1994; Jetz and Rubenstein, 2011; Rubenstein and Abbot, 2017). Habitat 29 specialist fishes on the other hand provide a unique opportunity to study social evolution as they often 30 reside in groups with low relatedness due to a pelagic larval phase (contrary to most terrestrial species; 31 Avise and Shapiro, 1986; Buston
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