The price of insurance: costs and benefits of worker production in a facultatively social bee

Behavioral Ecology The official journal of the ISBE International Society for Behavioral Ecology Behavioral Ecology (2018), 29(1), 204–211. doi:10.1093/beheco/arx146 Original Article The price of insurance: costs and benefits of worker production in a facultatively social bee Received 23 August 2017; revised 3 October 2017; editorial decision 9 October 2017; accepted 17 October 2017; Advance Access publication 17 November 2017. Kin selection theory is foundational in helping to explain the evolution of sociality; however, the degree to which indirect fitness benefits may underlie helping behavior in species of early stage sociality has received relatively little empirical attention. Facultatively social bees, which demonstrate multiple forms of social organization, provide prime systems in which to empirically test hypotheses regarding the evolutionary origins of sociality. The subsocial small carpenter bee, Ceratina calcarata, may establish a social nest by manipulating brood provisions to rear a worker daughter, which then assists in critical late-season alloparental care. Here, we combine nest demographic and behavioral data with genetic relatedness estimates to calculate the relative inclusive fitness of both subsocial and social reproductive strategies in C. calcarata. Social mothers benefit from improved likelihood of brood survivorship and have higher fitness than subsocial mothers. Worker daughters have low indirect fitness on average, and will not produce their own offspring. Among-sibling relatedness is significantly higher in social nests than subsocial nests, though mothers of either reproductive strategy may mate multiply. Though this study corroborates the ultimate role of indirect fitness and assured fitness returns in the evolution of social traits, it also offers additional support for maternal manipulation as the proximate mechanism underlying evolutionary transitions in early stage insect societies. Key words: assured fitness returns, Ceratina, facultative sociality, inclusive fitness, maternal manipulation, Social evolution. INTRODUCTION Eusociality is one of the most complex forms of social organization in nature (Wilson 1971). Although eusocial organisms are represented by a diverse suite of taxa (e.g., naked mole rats, Jarvis 1981; thrips, Crespi 1992; shrimp, Duffy 1996; termites, Thorne 1997), Hymenoptera collectively contain more eusocial species than any other group (Wilson 1971). Obligately eusocial bees (e.g., Apis mellifera) demonstrate complex reproductive division of labor. Each individual’s role within the colony is irreversibly determined during development, and a reproductive queen’s lifetime fitness depends on the collective effort of thousands of sterile workers (Wilson 1971; Wilson and Hölldobler 2005; Michener 2007). Despite their established ecological dominance, however, eusocial bees represent relatively few species. Most of the more than 20,000 bee species worldwide are solitary (Michener 2007) and the remainder demonstrate forms of noneusocial organization (Rehan and Toth 2015). Solitary nesting is ancestral in bees, but evidence suggests that lineages may undergo continuous evolutionary gains or losses in their social complexity (Szathmáry and Smith 1995; Danforth 2002; Rehan and Toth 2015). The evolutionary origins of an obligate and sterile worker caste Address correspondence to S.A. Rehan. E-mail: . thus appear paradoxical: why would an individual sacrifice its direct fitness to assist in rearing another’s offspring? Further, how might such a seemingly altruistic behavioral phenotype be selectively reinforced? Inclusive fitness theory suggests that indirect fitness benefits to the altruist may be enough to account for the origin and elaboration of the advanced eusocial worker caste (Hamilton 1964; West-Eberhard 1975; Trivers and Hare 1976; Foster et al. 2006). As formalized by Hamilton (1964), if an altruist’s helping behavior were to contribute to the direct fitness of close genetic relatives, its indirect fitness gains could outweigh the incurred costs of forgoing some or all of its own reproduction. Kin selection is thus considered a plausible explanation for the evolution of sociality in Hymenoptera, in which female siblings are expected to share significantly more of their genetic identity with each other compared to their mother or brothers (Hamilton 1972; Lin and Michener 1972). Though the multiple mating of advanced eusocial species appears to confound these expectations by reducing among-sibling relatedness (Palmer and Oldroyd 2000), monandry is thought to be ancestral to Hymenoptera and suggests indirect fitness could have facilitated the emergence of early stage social traits (Hughes et al. 2008). The biological applicability of kin selection has been the subject of heated debate within the field of social evolution (WestEberhard 1975; Wilson 2005; Gadagkar 2010; Nowak et al. 2010; Marshall 2011). While the maintenance and elaboration of © The Author(s) 2017. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: Wyatt A. Shell and Sandra M. Rehan Department of Biological Sciences, University of New Hampshire, 46 Academic Way, Durham, NH 03924, USA Shell and Rehan • Worker production in a facultatively social bee may be prompted by physical aggression rather than sibling relatedness in this group (Augusto and Garófalo 2004; Pech et al. 2008). Taken together, studies suggest that while ecological pressures and genetic identity among family groups likely help to maintain and even reinforce social traits through inclusive fitness, 1) social nesting may not be an advantageous strategy for all individuals involved; and 2) physical and/or aggressive interactions among nestmates may be required to elicit and maintain sib-social care behaviors (Ratnieks and Wenseleers 2008). Costbenefit analyses of facultatively social species are few, yet critical to understanding the underlying mechanisms for social organization in early stage societies. The small carpenter bee, Ceratina calcarata demonstrates a form of facultative incipient sociality across its range in eastern North America (Rehan and Sheffield 2011; Shell and Rehan 2016a) where it produces one brood per year (Johnson 1988; Rehan and Richards 2010b). All reproductively active female C. calcarata nest subsocially by providing extended parental care for their maturing brood. Some mothers, however, establish social nests by producing a worker daughter to assist with late-season brood feeding and defense (Figure 1; Rehan, Berens et al. 2014; Lawson et al. 2016). Maternal manipulation is thought to play an important role in C. calcarata’s nesting biology (Rehan and Richards 2013). Specifically, a reproductive female can choose whether to fertilize her eggs and, with carefully controlled pollen provisioning, can determine both the sex and body size of her (...truncated)