Fitness consequences of ecological constraints and implications for the evolution of sociality in an incipiently social bee

Biological Journal of the Linnean Society, 2011, 103, 57–67. With 4 figures Fitness consequences of ecological constraints and implications for the evolution of sociality in an incipiently social bee SANDRA M. REHAN1*, MICHAEL P. SCHWARZ2 and MIRIAM H. RICHARDS1 Department of Biological Sciences, Brock University, 500 Glenridge Avenue, St Catharines, Ontario, L2S 3A1, Canada 2 School of Biology, Flinders University, GPO Box 2100, Adelaide, South Australia 5000, Australia Received 5 December 2010; revised 15 January 2011; accepted for publication 15 January 2011 bij_1642 57..67 Ecological constraints such as resource limitation, unfavourable weather conditions, and parasite pressure have long been considered some of the most important selective pressures for the evolution of sociality. In the present study, we assess the fitness consequences of these three ecological factors on reproductive success of solitary nests and social colonies in the socially polymorphic small carpenter bee, Ceratina australensis, based on 982 nests collected over four reproductive periods. Nest site limitation was predicted to decrease opportunities for independent nest initiation and increase the frequency of social nesting. Nest sites were not limiting in this species and the frequency of social nesting was consistent across the four brood-rearing periods studied. Unfavourable weather was predicted to lower the frequency of female dispersal from their natal nests and to limit the brood-rearing season; this would increase the frequency and fitness of social colonies. Daily temperature and precipitation accumulation varied between seasons but were not correlated with reproductive success in this bee. Increased parasite pressure is predicted to increase the frequency and fitness of social colonies because solitary bees must leave the nest unattended during foraging bouts and are less able to defend the nest against parasites. Severe parasitism by a chalcid wasp (Eurytoma sp.) resulted in low reproductive success and total nest failure in solitary nests. Social colonies had higher reproductive success and were never extirpated by parasites. The high frequency of solitary nests suggests that this is the optimal strategy. However, social colonies have a selective advantage over solitary nesting females during periods of extreme parasite pressure, and we suggest that social nesting represents a form of bet-hedging against unpredictable fluctuations in parasite number. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103, 57–67. ADDITIONAL KEYWORDS: parasite pressure – resource limitation – small carpenter – polymorphism – temporal variation. INTRODUCTION Environmental conditions have the potential to greatly influence the survival and fecundity of individuals, and their importance has been stressed for the evolutionary origins and maintenance of social behaviour in cooperatively breeding vertebrates (Woolfenden & Fitzpatrick, 1978; Emlen, 1991) and invertebrates (Lin & Michener, 1972; Evans, 1977; Strassmann & Queller, 1989; Wcislo, 1997). A growing *Corresponding author. E-mail: number of ecological studies has linked group living to constraints in species’ biotic and abiotic environments and has found that resource limitation, climate and predation pressure can all play roles in selection for social behaviour. Although the importance of ecological factors has been emphasized for the evolution of social groups, there are few empirical studies tracking the selective pressure imposed by ecological constraints on both solitary individuals and social group fitness in sympatry. First, depending on species and environment, resources can vary in abundance and ease of acquisition. The basic necessary resources are breeding © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103, 57–67 57 1 58 S. M. REHAN ET AL. resulted in nest flooding, which led to brood rot resulting in high nest failure and low brood survival rates. Atypically warm weather resulted in an early onset of brood production, larger clutch sizes and, in turn, higher rates of worker oviposition (Richards, Packer & Seger, 1995) because worker numbers and pollen collection exceeded the queen’s egg-laying abilities. To our knowledge, no studies have contrasted a socially polymorphic species, with both solitary and social nests in the same population, over a series of brood-rearing periods to investigate how these sources of ecological variation might select for variation in social behaviour. The role of fluctuating environmental conditions has long been considered important for social insects and vertebrates but direct tests have been few (Strassmann & Queller, 1989; Emlen, 1991; Wcislo, 1997; Purcell, 2010). Elucidating the environmental conditions that favour either solitary or social nesting strategies requires studying species in which both strategies occur in sympatry, so that the fitness consequences of each nesting strategy can be assessed over a series of brood-rearing periods. The Australian small carpenter bee, Ceratina australensis, is socially polymorphic (Michener, 1962; Rehan, Richards & Schwarz, 2010), with both solitary and social nests in the same population; thus, seasonal and social variation can be compared to examine fitness consequences of solitary and social reproductive strategies. In solitary nests, females forage and reproduce independently. In social colonies, a primary female behaves much like a solitary female, taking on foraging and reproductive duties, whereas a secondary female remains at the nest as a passive guard and delays reproduction until the next season (Rehan et al., 2010). Females that disperse after eclosion to initiate new nests do so solitarily; however, females that reuse their natal nest may form social colonies. Adult females of this species often survive long enough to be reproductive in two consecutive brood-rearing seasons, either spring then summer, or summer then spring (Rehan et al., 2010). Ceratina mothers mass provision brood in a single linear burrow and, when oviposition is complete, mothers remain with their nests until the brood reach adulthood (Sakagami & Maeta, 1977). This nest loyalty ensures that the contents of complete nests are an appropriate measure of reproductive success because maternal investment and reproductive effort is constrained to a single stem (Rehan & Richards, 2010). The present study aimed to test predictions of temporal variation in three ecological factors (i.e. nest substrate availability, parasitism rates, and local weather) as influences on the expression of sociality and the fitness consequences for solitary and social © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103, 57–67 sites and food, and competition for scarce resources may promote cooperation and group living (Alexander, Noonan & Crespi, 1991). In insects, cooperati (...truncated)