Insect. Soc. (2016) 63:67–78 DOI 10.1007/s00040-015-0436-0 Insectes Sociaux

RESEARCH ARTICLE

Casteless sociality in an allodapine bee and evolutionary losses of social hierarchies

1 2,3 1 C. R. B. da Silva • M. I. Stevens • M. P. Schwarz

Received: 5 February 2015 / Revised: 24 August 2015 / Accepted: 7 September 2015 / Published online: 18 September 2015 Ó International Union for the Study of Social Insects (IUSSI) 2015

Abstract Communal behaviour is a form of social beha- that evolutionary periods involving reproductive hierarchies viour where two or more females nest together and have no could select for traits that allow individuals to better assess reproductive hierarchies. Communal behaviour has often their social environment and subsequently enable lower been regarded as an evolutionary ‘stepping stone’ to more reproductive skew. complex forms of sociality involving castes, as well as a social form derived from solitary behaviour with no further Keywords Communal Á Quasisocial Á Eusocial Á evolution towards eusociality. However, recent phyloge- Allodapini Á Casteless societies Á Reproductive skew netic studies on halictine bees suggest that some instances of communal behaviour are derived from eusociality. Here, we describe social nesting in an allodapine bee, Braunsapis Introduction puangensis, which has been introduced to Fiji from southern Asia. We show that this bee has a casteless form of sociality The evolution of complex insect societies with queen and similar to communal organization, but which has been worker castes, referred to as ‘eusociality’, has often resulted derived from an ancestrally hierarchical social system. This in enormous ecological success in descendant clades in ants, is likely due to a combination of small benefits for social termites, social wasps and some social bees (Wilson 1990, nesting that rapidly saturate as colonies become larger, 2008). As a result, there has been a strong focus on the along with low costs for dispersal. We suggest that casteless selective mechanisms that permit seemingly successful forms of sociality have frequently evolved from hierarchical forms of sociality to evolve only very rarely. Fu et al. (2015) societies across many insect groups, but the analyses argue that eusocial behaviour is risky and rewarding, which required for recognizing such societies are often undevel- is why it is taxonomically rare, whereas solitary reproduc- oped and hampers comparative approaches. Transitions tion is more conservative and common. At the same time, from hierarchical to casteless societies challenge the notion there have been origins of eusociality that have not led to that eusociality is an evolutionary ‘end point’ and we argue obvious ecological predominance, and these examples that eusociality can, in some cases, be regarded as an evo- include thrips (Kranz et al. 1999), aphids (Shibao 1998), lutionary step towards egalitarian societies. We also suggest bees (Schwarz et al. 2007) and mammals (Jarvis 1981; Clarke and Faulkes 2001). There has understandably been considerable debate around the selective processes leading & C. R. B. da Silva to the extreme forms of altruism in eusocial taxa (e.g. Keller dasi0009@flinders.edu.au and Reeve 1994; Queller and Strassmann 1998; Powell and 1 Biological Sciences, Flinders University, GPO Box 2100, Franks 2005), including the question of whether inclusive Adelaide, SA 5001, Australia fitness theory (Hamilton 1964) and associated reproductive 2 South Australian Museum, North Terrace, GPO Box 234, skew models (e.g. Reeve and Keller 2001) are sufficient or Adelaide, SA 5000, Australia not to explain the evolution of eusociality (e.g. Stevens et al. 3 School of Pharmacy and Medical Sciences, University of 2007; Nowak et al. 2010; Abbot et al. 2011; Boomsma et al. South Australia, Adelaide, SA 5000, Australia 2014). 123 68 C. R.B. da Silva et al.

Crespi (2009) has argued that ‘top-down’ approaches to less hierarchical societies or solitary living than had been social evolution, where theoretical models are used to previously thought (Brady et al. 2006; Cardinal and Dan- generate complex predictions that are difficult or impossible forth 2011; Rehan et al. 2012). It has been argued that losses to test, might be better replaced with ‘bottom-up’ approa- of eusociality are more likely to help us understand social ches where populations and taxa can be grouped in terms of evolution than gains, because the former transitions appear their life history, social structure and ecological traits. to be much more frequent (Michener 1985; Rehan et al. Crespi argues that instances of evolutionary convergence or 2012). divergence among these categories can be used to assess Among the bees, there are multiple known origins of broader theories. However, this approach requires that eusociality, though the actual number will depend on how forms of social organization can be identified using rigorous one defines eusociality (Kocher and Paxton 2014). For criteria, so that transitions in social structure can be confi- halictines, Gibbs et al. (2012) estimate two origins of dently inferred. eusociality and in comparison Danforth (2002) suggests that Debates on the origins of eusociality co-occur with a there have been at least 12 losses. Recent analyses of evo- related issue about ‘pre-conditions’ that might be required lution of social behaviour within halictines also suggest that for transitions into eusociality from less complex forms of the number of losses may be even higher (Gibbs et al. 2012). organization (e.g. Lin and Michener 1972; Kukuk 1992; Rehan et al. (2012) show that social living is ancestral for Kukuk et al. 1998; Wilson and Ho¨lldobler 2005; Wilson the Xylocopinae and has been lost in the Manueliini, mul- 2008; Wcislo and Tierney 2009). This latter issue is not tiple times in the carpenter bees (Xylocopini) and small inconsequential; the origins of eusociality have been carpenter bees (Ceratinini), though there are no transitions famously regarded as one of the very few major evolu- to strictly solitary living in the Allodapini (Chenoweth et al. tionary transitions in the evolution of life, because they shift 2007). the unit of selection from individuals to groups (Szathma´ry Allodapine bees are ideal organisms for exploring social and Smith 1995, 1997). If it turns out that eusocial species evolution; they have a wide range in forms of social orga- can evolve into more egalitarian societies, we may need to nization, ranging from mostly subsocial to highly eusocial reconsider the nature of transitions between forms of social (Schwarz et al. 2007). Allodapines progressively provision organization. their brood and differ from all other stem nesting bees that Some past studies argue that communal or casteless mass provision their brood in a series of cells (Michener societies are an unstable state between eusocial and solitary 2007). The allodapine genus Braunsapis occurs throughout behaviour. For example, Richards et al. (2003) suggest that Australia, southern Asia and Africa, and has an ancestral Halictus sexcinctus demonstrates a form of communal form of sociality involving reproductive queues (Schwarz behaviour that is an unstable transition between eusocial to et al. 2011). These queues comprise a hierarchical system solitary behaviour. On the other hand, Danforth and Ji where the oldest female within a nest lays eggs and provi- (2001) have argued that the widespread occurrence of sions the resulting brood, and younger females take on these communal behaviour in Australian Lasioglossum (Knerer roles when the dominant female dies or senesces (Joyce and and Schwarz 1976, 1978) represents the retention of Schwarz 2007). Such reproductive queues are common in ancestral behaviour present in the common ancestor of the allodapines, but in some lineages they have evolved into clade. The crown age of the Australian Lasioglossum clade queen/worker castes where non-reproductive roles are more has been dated to the late Oligocene (Gibbs et al. 2012), or less permanent (Schwarz et al. 2005, 2011; Dew et al. which therefore argues against communal behaviour as an 2012). evolutionarily unstable state in this group. Communal Here, we examine the social and nesting biology of the behaviour has also been reported from a wide variety of recently introduced allodapine bee Braunsapis puangensis other major clades in the Halictidae, including the Halictini to Fiji (da Silva et al. 2015) and show that it has lost a (e.g. Packer 1998; Danforth 1999; Timmermann and Kuhl- hierarchical system and evolved a ‘casteless’ social strat- mann 2008), Rophitinae (e.g. Rozen and McGinley 1976) egy. We argue that such transitions warrant much more and Nominae (e.g. Vogel and Kukuk 1994) and also for the attention than they have currently received. bee family Andrenidae (e.g. Paxton et al. 1996) and the apid tribe Euglossini (Cameron 2004). There is evidence that communal behaviour, in the halictids at least, can arise from Materials and methods both solitary and eusocial ancestors (Gibbs et al. 2012). Recent molecular phylogenetic studies have greatly Field sites changed our understanding of the origins of eusociality. Very broadly, these studies suggest far fewer origins of Braunsapis puangensis was sampled from the southern eusociality and many more transitions from eusociality to coast of Viti Levu, Fiji, from managed gardens and roadside 123 Casteless sociality in an allodapine bee and evolutionary losses of social hierarchies 69 vegetation where bees were nesting in pruned bushes and 2012). Non-parametric statistics were used for most analy- hedges of herbaceous plants. Nests were collected from the ses, because data were often strongly zero or one-truncated, Laucala Bay Campus of the University of the South Pacific, or were otherwise not normally distributed as determined by Suva, from 10th to 13th of July 2013, 15th to 18th of QQ plots (results not shown here). Kruskal–Wallis tests October 2013 and 18th to 21st of May 2014 (GPS coordi- were used to determine if there were significant differences nates 18°8051.4600S, 178°26058.2500E). Nests were also when treatments were nominal with [2 groups and depen- collected from Pacific Harbour, Viti Levu, on the 23rd of dent variables were scalar, and Mann–Whitney U tests were May 2014 (18°14053.6200S, 178°4050.7000E). Intact nests used when only two groups were being compared. When it were acquired at dawn and dusk to ensure all members of was necessary to estimate 95 % confidence limits for each nest were present when collected (i.e. not absent from parameters of scalar variables, we used bootstrapping with the nest while foraging). Nests were collected from dead 1000 pseudoreplicates, implemented in SPSS 21.0. stems of several herbaceous shrubs, including Bouganvillea Per capita brood production is a measure of colony sp., Bambusa sp. and Rosa sp. in 2013, while 2014 sample brood-rearing efficiency (Michener 1964; Schwarz 1988, nests were predominantly collected from Mussaenda ery- 1994) and its relationship with nest length and numbers of throphylla (Rubiaceae). adult females per nest was examined using generalized Nest entrances were only found at the dead terminal ends linear models (GLM), with a maximum likelihood approach of branches, which was often the by-product of horticultural used to estimate parameters and 1000 bootstrap pseu- pruning. Nest entrances were closed over with tape and doreplicates to measure b, an indication of the strength of nests were refrigerated to minimize bee activity until pro- the relationship between scalar variables. cessing, when the contents of each nest were removed and Lastly, we explored whether reproductive or foraging preserved in 99 % ethanol. Processing occurred within division of labour was apparent within nests using a Monte 3 days of field collection. For each colony, the numbers of Carlo approach. These simulations were used to see if eggs, larvae, pupae, callows and mature adults were recor- socially nesting females exhibited patterns of wing wear and ded. Nest lengths were recorded for the 2014 samples only. ovary size that were different from those expected for Per capita brood production (PCBP) was calculated as the solitary nesting females. Ovary size, used as an indicator of total number of brood present in a nest (including callows) reproductive status, and wing wear, an indicator of foraging divided by the number of adult females, and is used as a frequency, were ranked within colonies and analysed for broad measure of how brood-rearing efficiency varies with two-female nests using Monte Carlo simulation based on the the number of adult females. methods of Spessa et al. (2000) and Tierney et al. (2013)in the software platform R version 2.15.0. Firstly, mean dif- Dissections ferences in ovary size and wing wear for nestmates from two-female nests were calculated. These same females, Adult females were immersed overnight in 70 % ethanol to pooled across all two-female nests in the sample, were then reduce brittleness of internal organs and dissected under a allocated randomly into dyads to create the same number of stereomicroscope. Forewing length, measured as the dis- ‘virtual nests’ as in the actual field sample, using sampling tance from the axillary sclerites to the apex of the marginal without replacement, and we calculated the mean differ- cell, was used as a proxy of adult body size, as a previous ences for these dyads. This was repeated 10,000 times and study on the allodapine bee Exoneura robusta found that this the means from each simulation were used to develop a trait varies linearly with pupal weight (Schwarz 1986). Wing histogram of the expected differences under random pair- wear was measured as the number of nicks and tears in the ing. The observed mean differences were then compared distal margins of the forewings and this measure of wear has with these distributions and the proportion of simulated been correlated with both age and foraging activity in other samples that were greater than the actual field sample was allodapine species (e.g. Joyce and Schwarz 2006; Tierney calculated. This proportion was used to assess whether the and Schwarz 2009). Ovary size was measured as the summed observed differences between nestmates were significantly lengths of the three largest oocytes (Schwarz 1986). Sper- different from randomly sampled socially nesting females. mathecal status was determined by observing the opacity of As a further investigation, random pairs of females were spermatheca; if opaque the female is likely to be insemi- constructed from single-female nests and compared to the nated, if clear the individual is unmated (Schwarz 1986). ovary size and wing wear differences in two-female nests over 10,000 simulations. These analyses were conducted to Statistical analysis determine whether ovary size and wing wear differences in actual multi-female nests were different from expectations Statistical analyses were carried out using SPSS Statistics where two-female colonies comprised random associations 21.0 (IMB, Chicago) and R version 2.15.0 (R core team of single-female nests. Further evaluation of the presence of 123 70 C. R.B. da Silva et al. reproductive division of labour between nestmates was and the Laucala Bay locations in May 2014 (Mann–Whit- examined by Wilcoxon signed ranked tests to examine ney test, U = 892.0, P = 0.468). The Pacific Harbour covariance between ovary size, wing wear and body size sample (n = 67) comprised 25 single-female nests, 22 two- among ranked adult females. female nests, 16 three-female nests, three four-female nests and one five-female nest, while the Laucala Bay site (n = 26) contained 13 single-female nests, four two-female Results nests, eight three-female nests and one four-female nest. Only 65.7 % of single-female nests (n = 67/102) across Colony compositions all seasons contained brood, while 98.8 % of multi-female nests (n = 81/82) had brood. We did not compare rates of A total of 202 nests were collected from three sample broodless nests for multi-female colonies across samples, periods: 35 nests were collected in the middle of the dry because only a single multi-female nest lacked brood, but a season (July 2013); 51 nests at the end of the dry season Chi-square analysis indicated that rates of broodlessness did (October 2013); and 116 nests at the end of the wet season not differ across samples for single-female nests 2 (May 2014). There was a significant difference in the (X2 = 2.339, P = 0.310). The proportion of single females number of adult females per nest among these samples, in the May sample (n = 45/116) was significantly different ranging from solitary nesting females to a single nest from July (Mann–Whitney test, U 992.5, P \ 0.001) and comprising five adult females (Kruskal–Wallis test, October (U = 1676.0, P = 0.002), but these two latter 2 X2 = 22.94, P \ 0.001), where May 2014 was found to samples did not differ from each other (U = 587.5, have the most adult females per nest (Fig. 1). July 2013 had P = 0.146). a mean number of 1.1 females per nest, whilst there were The mean numbers of different brood stages (eggs, larvae, 1.25 females per nest for October 2013 and 1.8 for May pupae and callows) per nest for each sampling period are 2014. The distribution of colony sizes in our three samples summarized in Fig. 2, where 95 % confidence intervals were is indicated as a clustered bar chart in Fig. 1. While the estimated using 1000 bootstraps. Whilst these CI values mean number of females per nest during July 2013 and indicate that mean numbers for some developmental stages October 2013 was not significantly different (Mann–Whit- varied across the samples, when brood stages within each ney U test, U = 852.5, P = 0.675), both of these samples nest were converted into proportions of the total brood in differed from the May 2014 collection (Mann–Whitney each nest, Kruskal–Wallis tests showed that these propor- tests, U = 1200.0, P \ 0.001 and U = 1977.5, P \ 0.001 tions did not differ significantly across the three collection for both comparisons). The number of adult females per nest was not significantly different between the Pacific Harbour

Fig. 2 Error bar graph displaying the mean number of Braunsapis puangensis brood stages (e eggs, l larvae, p pupae and c callows) per Fig. 1 Bar chart showing colony size (number of adult female nest across the sample periods: July, October and May. Error bars nestmates) distributions of Braunsapis puangensis for each of the indicate 95 % confidence intervals determined from 1000 bootstrap sampling periods, July 2013, October 2013 and May 2014 pseudoreplicates 123 Casteless sociality in an allodapine bee and evolutionary losses of social hierarchies 71

2 2 periods (X2 = 5.125, P = 0.077; X2 = 1.341, P = 0.512; Per capita brood production 2 2 X2 = 4.366, P = 0.113; and X2 = 4.366, P = 0.113 for eggs, larvae, pupae and callows, respectively). However, The benefits gained by social nesting were explored by total brood sizes varied significantly across the samples examining per capita brood production (PCBP). Studies on 2 (Kruskal–Wallis test, X2 = 24.894, P \ 0.001). Pairwise other allodapines have suggested that prevention of brood Mann–Whitney tests indicated that May 2014 (mean total loss is a major benefit of social nesting, but for some species brood per nest = 7.42) had a significantly larger total brood there are further benefits from increasing PCBP once brood per nest compared to July 2013 (mean = 2.2) and October loss is taken into consideration (Bull and Schwarz 2001; 2013 (mean = 3.4) (Mann–Whitney test July 2013 and May Thompson and Schwarz 2006). We explored this possibility 2014, U = 1033.0, P \ 0.001, and Mann–Whitney test for our data by removing nests that lacked brood and then October 2013 and May 2014, U = 1981.0, P = 0.001), but used Kruskal–Wallis tests to examine whether PCBP varied with no difference in the total brood production per nest with the number of nestmates for each of the three seasonal between July 2013 and October 2013 (Mann–Whitney test, samples. These tests indicated no colony size effects (July, 2 2 U = 779.5, P = 0.306). X2 = 0.319, P = 0.852; October, X3 = 6.900, P = 0.075; 2 Proportions of brood developmental stages within single- May, X4 = 4.767, P = 0.312), and mean PCBP values with and mutli-female nests were examined to determine whe- bootstrap 95 % confidence intervals are shown in Fig. 3. ther single-female nests had a younger brood (e.g. eggs and The number of adult females found per nest and their larvae rather than pupae and callows). No significant dif- associated mean and median PCBP are shown in Table 1. ferences were found between single- and multi-female nests However, when nests lacking any brood at all were for any brood developmental stage (Mann–Whitney tests, proportion of eggs, U = 2698.0, P = 0.951; proportion of larvae, U = 2435, P = 0.281; proportion of pupae, U = 2402.5, P = 0.218; proportion of callows, U = 2402.5, P = 0.218). During nest content analysis, we found some single females with mature brood (pupae). We explored whether these females were the mothers of those mature brood, or instead had inherited their nest along with brood from pre- vious females who had since disappeared. If solitary nesting females are recent foundresses, rearing only their own brood, we would expect them to have proportionally fewer mature brood (pupae) than multi-female nests which must have already reared some brood to maturity. We therefore compared the proportion of pupae among brood for single and multi-female nests using a generalized linear model (GLM) with a maximum likelihood estimation of parame- ters. This was carried out separately for each of the three seasonal samples and we only included nests with at least Fig. 3 Mean per capita brood production as a function of the number one brood to exclude the effects of possible brood loss via of Braunsapis puangensis adult females per nest for each of the three sample periods. Error bars represent 95 % confidence intervals based parasites of predators. These analyses indicated no effect of on 1000 bootstrap pseudoreplicates and nests with more than three single-female versus multi-female for any of the samples adult females were excluded because of very small sample sizes 2 2 (likelihood ratio X1 = 0.059, P = 0.808; X1 = 2.234, 2 P = 0.135; and X1 = 0.082, P = 0.775 for the July, October and May samples respectively). Consequently, our Table I The number of adult females found per nest and their asso- ciated mean and median per capita brood production results do not suggest that, overall, single-female nests are substantially younger than multi-female nests, suggesting Number of Sample Mean number of Median number of adult females size (n) brood produced brood produced that some solitary nesting females represent brood that reached maturity in that nest, rather than being foundresses. 1 102 3.02 2 We then examined wing wear of solitary nesting females 2 40 7.2 6 with mature brood (pupae) in their nests. We found that 3 35 12.3 10 30.4 % (7/23) of single females with no wing wear at all had 4 5 9.8 4 pupae in their nest and it therefore seems very unlikely that 5 2 19.5 5 those pupae were their offspring. 123 72 C. R.B. da Silva et al. excluded, this relationship no longer occurred (Kruskal– 2 Wallis test, X2 = 1.694, P = 0.792). Despite the above results, when opening nests we noticed that many multi-female nests appeared to be extremely crowded with brood. We therefore explored whether nest length might limit brood-rearing efficiency for larger colo- nies. QQ plots (not shown here) indicated that PCBP, total brood numbers and the number of adult females were not normally distributed. We therefore used a generalized linear model (GLM) approach to examine how nest length and the number of adult females per nest influenced PCBP as covariate predictors. Nest length data were only available for the May 2014 sample. For our analyses, we used a maximum likelihood approach to estimate parameters and 1000 bootstrap pseudoreplicates to estimate 95 % profile likelihood confidence intervals of b for both predictor variables. This analysis indicated a significant positive effect of nest length (b = 0.500, likelihood ratio 2 X1 = 38.439, P \ 0.001, 95 % CI = 0.407–0.734), but a negative effect of the number of females (b =-0.880, 2 likelihood ratio X1 = 9.567, P = 0.002, 95 % CI =-1.430 to -0.331). To visualize the above results, we carried out two further GLM analyses, with each using only a single predictor covariate (nest length or the number of adult females) and using the same GLM settings. For each analysis, we then plotted the raw residuals against the predictor variable not used in the GLM (i.e. when nest length was used as a pre- dictor of PCBP), and the resulting residuals were then plotted against the number of adult females, and vice versa. The two resulting scattergrams are given in Fig. 4 and make apparent the opposing effects of nest length and adult females on PCBP when each predictor variable is taken into Fig. 4 Scattergram of raw residuals of per capita brood production account. (PCBP) after generalized linear modelling on nest length plotted against the number of adult females per nest (top panel), and raw residuals after GLM regression on adult females plotted against nest Absence of caste-like behaviour length (bottom panel). The scattergrams show that nest length and adult females have opposing effects on colony-rearing efficiency An analysis of the covariation between ovary size, wing wear and body size within nests was used to explore whether Monte Carlo simulations were also used to examine if there is any evidence for caste-like behaviour or behavioural reproductive hierarchies were apparent between nestmates. specialization. In two-female nests, females with the largest When ovary sizes chosen from females in two-female nests and smallest ovaries did not differ significantly in body size were randomly allocated into ‘simulated’ two-female (Wilcoxon signed ranked test, Z =-0.267, P = 0.789). colonies and then ovary size differences were calculated, we However, the level of wing wear for females with the largest found that 8261 of 10,000 random combinations had greater mean ovary size was marginally significantly greater than mean ovary size difference than the observed actual pairs. that of females with smaller mean ovary size (Wilcoxon Therefore, empirical samples showed no evidence of a signed ranked test, Z =-2.030, P = 0.042). In the 21 significant difference in ovary sizes between actual nest- three-female nests in our samples, there was no significant mates compared to random pairs. Ovary size data from difference in body size or wing wear between the female single-female nests were also used to generate a null dis- with the largest and the smallest mean ovary size (body size: tribution of 10,000 randomly paired females, and 5833 of Wilcoxon signed ranked test, Z =-1.231, P = 0.218; these were greater than the observed mean, similarly indi- wing wear: Wilcoxon signed ranked test, Z =-1.067, cating that the mean difference in ovary size between actual P = 0.286). nestmates is not significantly different to values expected 123 Casteless sociality in an allodapine bee and evolutionary losses of social hierarchies 73

variation in body size, ovary size and wing wear for two- female colonies was not different from expectations based on randomly generated ‘virtual’ colonies based on data from single-female nests. Furthermore, we found only a slight association between ovary size and level of wing wear, and many females with undeveloped ovaries had moderate levels of wing wear, suggesting foraging activities. Studies in some wasp species, such as Cerceris fumipennis, suggest that wing wear is not an effective way to reliably estimate age or task performance, but is more likely to be a result of a variety of traits (Nalepa 2012). However, multiple studies across allodapine genera suggest that high levels of wing wear do correspond with foraging activities rather than life history traits (Melna and Schwarz 1994; Joyce and Schwarz 2006, 2007; Schwarz et al. 2005). Insemination rates for social nests tended to be greater than for single-females, but Fig. 5 Box plot showing the number of adult females positively insemination status had no effect on mean ovary size. identified as being inseminated as a function of colony size. Data do Combined, our analyses indicate a lack of behavioural not include females whose insemination status was ambiguous, so castes, such as when egg-laying and foraging roles are insemination numbers are minimal estimates positively or negatively associated with each other, or indeed any associations of these with relative body size. Our from random assignment of single females into ‘virtual’ results therefore strongly suggest that B. puangensis in Fiji colonies. exhibits casteless societies with no apparent social hierar- Monte Carlo simulations using wing wear data from two- chies, but where adult females cooperate in nest use. female nests indicated that only 1832 from 10,000 random The ancestral form of sociality in allodapines comprises combinations were greater than the observed mean and sub- reproductive queues where older females adopt both egg- sequently were not significant (P = 0.183). Simulated dyads laying and foraging roles and, as they die or senesce, are based on data from single females produced 2704 from 10,000 then replaced in these tasks by younger females (Schwarz random combinations that were greater than the observed et al. 2011). This form of sociality has been replaced by mean, which also indicates that differences among actual eusociality in two arid-adapted species, Exoneurella tri- nestmates is not significantly different (P = 0.270) than if dentata and Hasinamelissa minuta, which exhibit distinct they comprised random assemblages of solitary females. queen and worker castes (Dew et al. 2012). Our results here More than one adult female per nest was inseminated for indicate that reproductive queues can also be replaced by many multi-female nests. We found medians of 1.5, 2 and 3 casteless organization. Reproductive queues can therefore inseminated females per nest for nests containing 2, 3 and 4 provide a starting point for the evolution of eusociality as female nestmates (Fig. 5), but because insemination status well as egalitarian societies, and raise the question of how could not be determined for all females (n = 24 undetermined and why age-based hierarchies could evolve into very dif- females) these values could be underestimates of the true ferent outcomes, one showing extreme reproductive skew number of inseminated females per nest. The mean ovary sizes and the other being casteless. of inseminated females were not different from uninseminated females when all females were combined (Mann–Whitney Life history and opportunities for alloparental care test, U = 4553.0, P = 0.811). When single-female nests were excluded, the insemination status did not affect the mean Our samples covered three widely separated seasonal peri- ovary length (Mann–Whitney test, U = 2199.5, P = 0.786). ods and indicate that the total number of brood varies with season, with the largest brood sizes occurring in May cor- responding to the end of the wet season. This is not Discussion surprising and rainfall-related patterns of brood size have been found for other tropical and subtropical bees (e.g. Social organization Joyce and Schwarz 2007; Tierney et al. 2013). Furthermore, the number of tree species flowering in the Suva region Our analyses did not indicate the existence of social hier- during the peak of the wet season (March) is almost triple archies that correspond to caste-like behaviour. Instead, the number flowering over the dry season (June–October) Monte Carlo simulations indicated that intra-colony (Ash 1992), so the greater number of adult females in our 123 74 C. R.B. da Silva et al.

May sample might reflect greater rates of brood rearing and female nests contained brood. This suggests that solitary maturation over the preceding wet season. Nevertheless, our nesting females are less able to protect their brood from data indicate year-round egg laying, as well as development predators, but it could also be a consequence of the recent and maturation of brood. This very protracted brood dispersal of solitary foundresses that have not yet produced development leads to year-round opportunities for females brood. However, the latter seems unlikely given the lack of to engage in alloparental care. The existence of single-fe- a difference in nest lengths of solitary females that had male nests with advanced (pupal) brood stages, but with low either some brood or no brood at all. We also found that the or zero wing wear suggests that there are indeed instances proportions of different brood stages within colonies with where females care for brood that are unlikely to be their brood did not vary significantly in social and solitary nests, own offspring and do so in the absence of other females who suggesting that solitary nests were not obviously younger could potentially coerce such altruism. than social nests. Our data also suggest that females could disperse from The above considerations suggest a clear benefit to social natal nests and commence egg laying throughout the year, nesting in terms of preventing brood loss. Fiji has a very which is very different from temperate and xeric allodap- abundant and diverse ant fauna (Ward and Wetterer 2006), ine species where egg-laying and brood-rearing periods are and one endemic ant species Cardiocondyla nuda was fre- seasonally constrained (Schwarz et al. 2007). Schwarz quently found nesting in the same shrubs used for nesting by et al. (2011) have argued that seasonally constrained B. puangensis and may have been the cause of brood loss brood-rearing periods could select for worker-like strate- whilst the solitary female was absent from the nest. Ants are gies, because any subordinate females precluded from known predators of allodapine brood and have the potential reproduction during a brief window of opportunity would to decrease the reproductive success of solitary nesting have a long latency to reproduction in the next window, females (Zammit et al. 2008). and this could select for altruism via assured fitness return Our results also indicate that when nests lacking any models (e.g. Queller and Strassmann 1998). Our samples brood were excluded from analyses, the number of adult suggestitisunlikelythatsuch constraints operate for B. females per nest had a significantly negative influence on puangensis. per capita brood production (PCBP), whilst nest length had Lastly, the influence of life history patterns on social a positive effect. This result was unexpected because in evolution will also depend on relatedness among nestmates. many allodapine species, colony size positively affects We were not able to estimate relatedness using genetic PCBP (e.g. Schwarz 1988, 1994; Tierney et al. 2000; Joyce markers in our study. However, cofounding of new nests in and Schwarz 2006). However, we found that the lengths of allodapines by more than one female has only ever been many nests in our samples were limited by the junction of a reported for the Australian genus Exoneura, despite inten- stem to a branch where woody junctions could not be tun- sive studies of other genera, including Braunsapis,in nelled through. Multi-female colonies in these ‘curtailed’ Africa, Madagascar and Australia (Schwarz et al. 2007). It is nests frequently had very densely packed brood, and it is therefore very likely that new nests in B. puangensis are possible that overcrowding of brood could have reduced founded by solitary females. However, subsequent recruit- colony-rearing efficiency. As allodapine nests are linear and ment of new females to colonies, via brood maturation is have tunnel diameters that are not much larger than a mature likely to lead to complex kinships among nestmates because larva, short nests containing many broods could make it of generational overlap and the existence of multiple difficult for adults to feed and groom large numbers of brood females contributing to brood, as has been found in other thus reducing brood-rearing efficiency. allodapines (e.g. Schwarz 1987; Schwarz et al. 1996; Har- Overall, our results indicate that the benefits of social radine et al. 2012). living are due to prevention of broodlessness and that these benefits saturate quickly. When these benefits are taken into Brood-rearing efficiency account, increasing colony size actually has a negative effect on brood-rearing efficiency. We interpret these results A review of allodapine species (Schwarz et al. 2007), shows as suggesting that social nesting involves a balance between that the number of brood per adult female tends to increase the positive effects of preventing broodlessness and avoid- with the number of adult females per nest across multiple ing the negative effects of overcrowding, and that the genera. Such benefits are derived from the prevention of tipping point between these two factors occurs at very small brood loss in multi-female nests, as well as increases in per colony sizes. The actual tipping point probably involves the capita brood production with increasing colony size (e.g. likelihood that multi-female nests would be buffered from Bull and Schwarz 2001; Thompson and Schwarz 2006; effects of reverting to a single-female nest following the loss Stevens et al. 2007). In our study, approximately 40 % of of an adult, and this is a benefit that would not show up in single-female nests lacked brood, whilst nearly all multi- our data. 123 Casteless sociality in an allodapine bee and evolutionary losses of social hierarchies 75

The evolution of casteless societies discussed above indicate that if eusociality is lost, solitary behaviour is not the only potential result and that casteless Species like B. punagensis provide opportunities to explore organization, such as communal and quasisocial groups, why selection on ancestral lineages with reproductive have arisen from hierarchical societies across multiple bee queues could lead to the extremes of species with effectively groups. Surprisingly, there have been very few attempts to sterile worker castes or else egalitarian societies. Our B. rigorously quantify the benefits of group living in casteless puangensis data suggest a situation where benefits from species, despite their obvious relevance for reproductive social nesting are small (but non-zero) and saturate for skew models (Reeve and Keller 2001). Kukuk and Sage colony sizes greater than two females, and where constraints (1994) found that reproductivity per female in the com- to independent nesting are low and not seasonally con- munal halictine bee, Lasioglossum hemichalceum, did not strained. These circumstances are consistent with models vary with group size and that there seemed to be few con- that predict low reproductive skew (e.g. Reeve and Keller straints to independent nesting; a result that is similar to 2001; Buston and Zink 2009), whilst the extreme caste what we find for B. puangensis and which is consistent with dimorphism in E. tridentata is consistent with strong sea- expectations from reproductive skew theory. At the same sonal and ecological constraints to independent nesting, time, Kukuk et al. (1998) found that a substantial proportion where subordinate females have very few opportunities for of females (approximately 60 %) in L. hemichalceum spring independent nesting (Dew et al. 2012). Kocher et al. (2014) nests did not forage, raising the question of whether this is a show that altitude and rates of brood development also truly egalitarian species. We argue that these considerations affect forms of sociality; highly social species develop more prompt three major issues, which we now briefly outline. quickly and can therefore reproduce during shorter seasons Firstly, our study and others discussed above are con- at high elevations than intermediate social taxa which have sistent with models that predict low skew when benefits of longer development times. Efforts are needed to see if these sociality and constraints to independent nesting are low. ecological conditions predict social transitions in other taxa. This holds the promise that skew models may be at least The evolution of communal societies from solitary ante- partially corroborated for casteless societies. Secondly, it is cedents has been inferred for multiple lineages. Barretto-Ko not trivial to show that casteless societies, which have been et al. (1996) showed that communal behaviour in Perdita assumed for some halictine communal species, are truly texana has been derived from a solitary state without involving egalitarian or lack reproductive hierarchies (Dew et al. a phase of eusociality, and origins of communal behaviour 2015). This issue is critical if ‘bottom-up’ approaches from solitary living also seem likely for some lineages of (Crespi 2009) to social evolution and reproductive skew halictid bees in the Rophitinae, the Nomiinae and the models are taken: ill-based assumptions about the existence Caenohalictini (Gibbs et al. 2012). However, transitions from of egalitarian or hierarchical structures could readily sug- socially hierarchical to more or less egalitarian societies have gest false patterns. Monte Carlo analyses can be used to at also been inferred in multiple lineages (e.g. Danforth and Ji least partially address this problem, but sample sizes need to 2001; Rehan et al. 2012; Gibbs et al. 2012). Gibbs et al. (2012) be large and patterns of colony phenology treated cau- proposed that communal nesting in Australian halictines is tiously. Unfortunately, many, if not most, empirical studies derived from an ancestral eusocial state and that communal that have implied communal or quasisocial organization behaviour in a Patellapis species (Timmermann and Kuhl- have not used analyses that can confidently demonstrate mann 2008)andinLasioglossum (Dialictus) figueresi (Wcislo egalitarian or casteless societies. Thirdly, our study and et al. 1993) may also be derived from eusocial ancestors. other recent studies raise the issue of why, once eusociality Hogendoorn et al. (2001) also argued that the Australian or other hierarchical forms of organization have evolved, allodapine species E. eremophila lost dominance hierarchies they can be lost and replaced by seemingly casteless forms from an ancestral eusocial state. In the corbiculate apids, of social organization. recent molecular studies suggest that communal behaviour in It has already been argued that eusociality should not be the Euglossini (e.g. Garo´falo et al. 1998) is derived from a seen as an ‘end point’ of social evolution, but rather as one eusocial ancestral corbiculate (Cardinal and Danforth 2011, of many possible strategies that can evolve to meet envi- but see Almeida and Porto 2015); however, eusocial behaviour ronmental challenges (e.g. Wcislo and Tierney 2009). We has been maintained in some genera of Euglossini as outlined raise the possibility that once hierarchical societies have by Cocom Pech et al. (2008). In contrast to these studies, there evolved, they may provide selection pressures for the is no evidence we are aware that eusociality has evolved from ability of individuals to assess their social environment and communal behaviour, as proposed in Michener’s ‘parasocial reduce despotism whilst maintaining benefits of social route’ (Michener 1969; Lin and Michener 1972). nesting. This suggests that in some cases, hierarchical Whilst Danforth (2002) has shown that eusociality is organization could be viewed as a stepping stone to frequently lost to solitary nesting, our study and others casteless societies. 123 76 C. R.B. da Silva et al.

Acknowledgments We thank Marika Tuiwawa, Apatia Liga and da Silva CRB, Groom SVC, Stevens MI, Schwarz MP (2015) Current Hilda Sakitiwaqa at the University of the South Pacific for providing us status of the introduced allodapine bee Braunsapis puangensis with laboratory and field support in Fiji. We also thank Simon Tierney (Hymenoptera: Apidae) in Fiji. Aust Entomol. doi:10.1111/aen. for providing us with the Monte Carlo script used in the program ‘R’ to 12149 analyse differences in ovary size and wing wear and Scott Groom for Danforth BN (1999) Phylogeny of the bee genus Lasioglossum allowing the 2013 collections available for analysis. We also thank (Hymenoptera: Halictidae) based on mitochondrial COI sequence Miriam Richards, the three anonymous reviewers, Simon Tierney, data. Syst Entomol 24:377–393. doi:10.1046/j.1365-3113.1999. Karen Burke da Silva, Jack da Silva and Owen Coffee for helpful 00087.x comments on earlier versions of this manuscript. 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