Climate-mediated behavioural variability in facultatively social bees

Biological Journal of the Linnean Society, 2018, 125, 165–170. With 2 figures. Climate-mediated behavioural variability in facultatively social bees SCOTT V. C. GROOM1,2 and SANDRA M. REHAN3* School of Agriculture, Food and Wine, University of Adelaide, Adelaide, South Australia, Australia Center for Ecological Research, Kyoto University, Kyoto, Japan 3 Department of Biological Sciences, University of New Hampshire, Durham, NH, USA 1 Received 24 May 2018; revised 27 June 2018; accepted for publication 28 June 2018 Social organisms are some of the most pervasive on earth, with the origin of sociality considered a major evolutionary transition. Previous studies suggest a role for both genetic and environmental factors in the transition from solitary to social living, with the relative contributions of these factors varying among taxa. Eusociality has arisen up to 11 times in the Hymenoptera. Four of these origins occurred within the bees, plus many probable reversions, making them ideal to understand the influence of genes and environment on social behaviour. We used a well-supported phylogeny with broad taxonomic coverage of the globally distributed bee genus Ceratina to test whether climate and sociality are correlated. Ceratina was most probably social ancestrally and originated in tropical Africa, with subsequent dispersals into temperate regions corresponding to shifts to solitary living. These findings highlight the utility of facultatively social lineages, such as Ceratina, for assessing the relative importance of phylogeny and ecology in the evolution of social complexity. ADDITIONAL KEYWORDS: Ceratina – ecological context – Hymenoptera – latitude – social behaviour – tropical INTRODUCTION Social organisms make up some of the most successful lineages on earth, yet eusociality has arisen only a few times (Wilson, 1971). Both genetic and environmental variation have been attributed to the evolution of social behaviour (Rehan & Toth, 2015), but empirical studies are few, and the relative contributions of phylogeny and selection vary among taxa (Jetz & Rubenstein, 2011; Purcell, 2011; Sheehan et al., 2015; Lukas & Clutton-Brock, 2017). To understand the influence of environment on the expression of social phenotypes, clades that exhibit lability in their sociality offer unrivalled potential for comparative study (Rehan & Toth, 2015). Behaviour may vary with environmental conditions, genotypes or genotype–environment interactions (Wong & Candolin, 2015), but a set of preconditions relating to both mother and nest longevity appears fundamental to social behaviour and the extent of plasticity (Andersson, 1984). Mothers that are long lived *Corresponding author. E-mail: can progressively provision and interact with mature offspring, and remaining loyal to a nest across time impedes predation and facilitates care to reduce offspring mortality (Sakagami & Maeta, 1977). In selective environments, these preconditions may enable cooperative behavioural responses that favour population persistence and the evolution of genetic modifiers that enhance their expression (West-Eberhard, 2003). Although species may possess all precursors for social behaviour to arise, the ecological context represents a strong predictive factor in its evolution. Comparative studies investigating congeneric and conspecific variation suggest that sociality closely tracks geographical and climatic gradients, with primitively social species more likely to be found at lower latitudes and elevations (Purcell, 2011). Social phenotypes may adapt to a broader range of conditions, enabling expansion of their distribution beyond the capacity of solitary nesting individuals (Sun et al., 2014; Brooks et al., 2017). The demands of both reproductive and foraging behaviours mean that environments presenting a combination of selective pressures, such as floral resource and nest site availability, are likely to be constraining for solitary nests in unpredictable conditions. © 2018 The Linnean Society of London, Biological Journal of the Linnean Society, 2018, 125, 165–170 165 2 166 S. V. C. GROOM and S. M. REHAN MATERIAL AND METHODS Ancestral state Ancestral state reconstructions were determined for key nodes of the phylogenetically robust maximum credibility tree produced by Rehan & Schwarz (2015) for Ceratina. These nodes represent either major biogeographical shifts or changes in sociality for key clades, summarized in the Supporting Information (Table S1). A character matrix allowing multiple states for 99 taxa was compiled for two traits: (1) sociality, simplified to either solitary or social (N = 34 species: eight solitary and 26 social); and (2) climate, reduced to temperate or tropical (N = 99 species: 18 temperate, 73 tropical and eight species that occur in both temperate and tropical climates; see Supporting Information, Table S2). Behavioural data for Ceratina largely comprise anecdotal observations (Sakagami & Maeta, 1977), which limited our classification of solitary taxa to only known obligate single foundress, including subsocial species, whereas social species included all varieties of multi-female cooperative nesting. Using the MultiState function in BayesTraits (Pagel et al., 2004), the two traits were mapped across 200 random postburn-in trees from Rehan & Schwarz (2015) to accommodate phylogenetic uncertainty. Analyses were repeated five times to account for potential instability in marginal likelihood estimation from the harmonic mean, which was assessed across each run to confirm stability. As the harmonic mean is a running total, the best run was determined through III 40 Mya 66.5° V 34 Mya IV 37 Mya 23.5° II I 56 Mya VII VI IX VIII 42 Mya 25 Mya 10 Mya 0° 26 Mya 6 Mya 23.5° Tropical Temperate 66.5° Figure 1. Map showing ages of Ceratina radiation through global climate zones. Ceratina had a tropical African origin, followed by cosmopolitan distribution. Species are currently distributed across both tropical and temperate biogeographical zones world-wide. © 2018 The Linnean Society of London, Biological Journal of the Linnean Society, 2018, 125, 165–170 Lineages that are facultatively social, where females are totipotent and capable of acting solitarily or as a social reproductive or helper, represent prime targets to uncouple the importance of genetic and environmental components in shaping the evolution of sociality. Bees of the genus Ceratina (Apidae: Xylocopinae) exhibit remarkable social variability, covering the full spectrum from solitary to eusocial behaviour, with numerous facultative social species. Ceratina are long lived and nest loyal, with mothers exhibiting prolonged mother–offspring interaction, often feeding young adults before overwintering or dispersal (Sakagami & Maeta, 1977). This genus originated in Africa ~56 Mya before radiating globally (Fig. 1) and comprises 17 Old World subgenera and six New World subgenera of ~200 described sp (...truncated)