Environmental barriers to sociality in an obligate eusocial sweat bee

Insectes Sociaux https://doi.org/10.1007/s00040-018-0642-7 Insectes Sociaux RESEARCH ARTICLE Environmental barriers to sociality in an obligate eusocial sweat bee P. J. Davison1,2 · J. Field1,2 Received: 22 March 2018 / Revised: 13 June 2018 / Accepted: 27 June 2018 © The Author(s) 2018 Abstract Understanding the ecological and environmental contexts in which eusociality can evolve is fundamental to elucidating its evolutionary origins. A sufficiently long active season is postulated to have been a key factor facilitating the transition to eusociality. Many primitively eusocial species exhibit an annual life cycle, which is thought to preclude the expression of eusociality where the active season is too short to produce successive worker and reproductive broods. However, few studies have attempted to test this idea experimentally. We investigated environmental constraints on the expression of eusociality in the obligate primitively eusocial sweat bee Lasioglossum malachurum, by transplanting nest foundresses from the south to the far north of the United Kingdom, far beyond the natural range of L. malachurum. We show that transplanted bees can exhibit eusociality, but that the short length of the season and harsher environmental conditions could preclude its successful expression. In one year, when foundresses were transplanted only after provisioning first brood (B1) offspring, workers emerged in the north and provisioned a second brood (B2) of reproductives. In another year, when foundresses were transplanted prior to B1 being provisioned, they were just as likely to initiate nesting and provisioned just as many B1 cells as foundresses in the south. However, the life cycle was delayed by approximately 7 weeks and nests suffered 100% B1 mortality. Our results suggest that short season length together with poor weather conditions represent an environmental barrier to the evolution and expression of eusociality in sweat bees. Keywords Sweat bee · Lasioglossum · Field transplant · Eusocial Introduction Determining how extrinsic environmental factors can affect the formation and persistence of social groups is critical to understanding the origin of complex social behaviours such as eusociality (Korb and Heinze 2008). The environment is thought to influence the geographic distribution and expression of social behaviour across a variety of vertebrate and arthropod taxa (Jetz and Rubenstein 2011; Purcell 2011; Faulkes and Bennett 2013; Sheehan et al. 2015, but see for example Gonzalez et al. 2013). Harsher or more variable Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00040-018-0642-7) contains supplementary material, which is available to authorized users. * P. J. Davison 1 School of Life Sciences, University of Sussex, John Maynard Smith Building, Brighton BN1 9QG, UK 2 Centre for Ecology and Conservation, University of Exeter, Penryn Campus, Cornwall TR10 9EZ, UK environments might favour social behaviour because independent nest founding is risky, or because the presence of multiple individuals can act as a buffer against challenging or unpredictable conditions (Jetz and Rubenstein 2011; Hoiss et al. 2012; Kocher et al. 2014; Sheehan et al. 2015). Eusociality is characterised by cooperative brood care and a reproductive division of labour (Wilson 1971), and considerable attention has been given to elucidating its evolutionary origins (see Bourke 2011). A perennial life cycle, nest thermoregulation, large colony size and food storage are derived characteristics of advanced eusocial insects such as ants and honeybees thought to favour eusociality in harsh environments (Kaspari and Vargo 1995; Hoiss et al. 2012; Wcislo and Fewell 2017). However, primitively eusocial bees and wasps, which lack morphological castes, and their solitary ancestors, typically complete an annual life cycle, form small groups and exhibit only limited nest thermoregulatory control (Cowan 1991; Reeve 1991; Potts and Wilmer 1997; Michener 2007). Thus, for primitively eusocial groups, eusociality may provide less buffering against environmental unpredictability. For example, workers can 13 Vol.:(0123456789) P. J. Davison, J. Field increase the chances of successfully rearing brood (e.g. Brand and Chapuisat 2014) but are of little value in years when conditions are so poor that offspring production is precluded altogether (Packer et al. 1989). Indeed, an annual colony cycle suggests both that the active season must be sufficiently long to sequentially produce workers and reproductives (Kocher et al. 2014), and that eusociality is inherently risky if any reproductive payoff is delayed until the end of the season (Fu et al. 2015). Consequently, season length and localized geographic and temporal environmental variation are thought to play significant roles in shaping inter- and intraspecific variation in social organization of primitively eusocial insects (Richards and Packer 1996; Fucini et al. 2009; Kocher et al. 2014). Sweat bees (Hymenoptera: Halictidae) exhibit considerable variation in social behaviour, from solitary nesting to primitive eusociality (Schwarz et al. 2007). This makes them an ideal group with which to examine the role of the environment during the early evolutionary stages of eusociality (Wcislo 1997). Eusociality in sweat bees is characterised by the presence of at least two broods: a first brood (B1) including some typically smaller female workers together with a variable proportion of males, and a second brood (B2) comprising reproductives only. It is thought that social behaviour can be expressed only where the season is sufficiently long to rear consecutive broods (Davison and Field 2016 and references therein), suggesting that sociality is temporally precluded where the season is too short (Kocher et al. 2014; but see Miyanaga et al. 1999). In at least one socially polymorphic sweat bee the expression of sociality is plastic, and the decision whether to become social may be associated with the amount of time remaining in the season after the emergence of B1 offspring (Field et al. 2010, 2012; see also Hirata and Higashi 2008). Variation in environmental conditions can strongly affect phenology, demography and colony social organisation (Packer et al. 1989; Richards and Packer 1996) by influencing the timing of nest initiation, foraging opportunities and rates of brood failure (Richards and Packer 1995; Richards 2004; Field et al. 2012; Richards et al. 2015). Furthermore, at least one socially polymorphic species is known to produce a greater proportion of B1 males in social nests situated further north (Yanega 1993). This might represent a bet-hedging strategy against the failure of B2, because mated B1 females can directly enter hibernation (Yanega 1989, 1993). Nevertheless, it remains to be demonstrated experimentally that a shorter season length completely precludes the persistence of primitive eusociality (Ko (...truncated)