Split sex ratios and genetic relatedness in a primitively eusocial sweat bee

Abstract

In eusocial Hymenoptera, queens and their helper offspring should favour different sex investment ratios. Queens should prefer a 1:1 investment ratio, as they are equally related to offspring of both sexes (r = 0.5). In contrast, helpers should favour an investment ratio of 3:1 towards the production of female brood. This conflict arises because helpers are more closely related to full sisters (r = 0.75) than brothers (r = 0.25). However, helpers should invest relatively more in male brood if relatedness asymmetry within their colony is reduced. This can occur due to queen replacement after colony orphaning, multiple paternity and the presence of unrelated alien helpers. We analysed an unprecedentedly large number of colonies (n = 109) from a UK population of Lasioglossum malachurum, an obligate eusocial sweat bee, to tease apart the effects of these factors on colony-level investment ratios. We found that multiple paternity, unrelated alien helpers and colony orphaning were all common. Queen-right colonies invested relatively more in females than did orphaned colonies, producing a split sex ratio. However, investment ratios did not change due to multiple paternity or the presence of alien helpers, reducing inclusive fitness pay-offs for helpers. Queen control may also have been important: helpers rarely laid male eggs, and investment in female brood was lower when queens were large relative to their helpers. Genetic relatedness between helpers and the brood that they rear was 0.43 in one year and 0.37 in another year, suggesting that ecological benefits, as well as relatedness benefits, are necessary for the maintenance of helping behaviour. Significance statement How helping behaviour is maintained in eusocial species is a key topic in evolutionary biology. Colony-level sex investment ratio changes in response to relatedness asymmetries can dramatically influence inclusive fitness benefits for helpers in eusocial Hymenoptera. The extent to which helpers in primitively eusocial colonies can respond adaptively to different sources of variation in relatedness asymmetry is unclear. Using data from 109 colonies of the sweat bee Lasioglossum malachurum, we found that queen loss, but not multiple paternity or the presence of alien helpers, was correlated with colony sex investment ratios. Moreover, we quantified average helper-brood genetic relatedness to test whether it is higher than that predicted under solitary reproduction (r = 0.5). Values equal to and below r = 0.5 suggest that relatedness benefits alone cannot explain the maintenance of helping behaviour. Ecological benefits of group living and/or coercion must also contribute.

Linked supergenes underlie split sex ratio and social organization in an ant

“…Subsequent studies (reviewed in refs. 37 , 39 , and 40 ) tested four scenarios that increase the variation in relatedness asymmetry among colonies, including variation in queen number ( 41 – 46 ), variation in queen insemination ( 41 , 42 , 45 , 47 ), variation in breeder turnover ( 46 , 48 – 50 ), and presence or absence of workers ( 51 ), as well as two scenarios not involving relatedness asymmetry, namely resource availability ( 43 , 52 – 54 ) and maternally inherited parasites ( 55 , 56 ). Ants in the genus Formica emerged as a prominent model system, as a result of their widespread and well documented variation in sex ratio and social structure ( 35 ).…”

Sisters doing it for themselves: extensive reproductive plasticity in workers of a primitively eusocial bee

“…B1 females emerge in early summer and provision the B2 generation of reproductive offspring (Packer and Knerer 1985;Schwarz et al 2007). In a third of colonies in our study population, the foundress dies during the B2 provisioning stage (Pennell and Field 2021). The B2 generation mate upon emerging from the nest.…”

“…In advanced eusocial taxa such as honeybees and ants, there is often extreme morphological differentiation, sometimes including irreversible helper sterility (Bourke and Franks 1995;Peeters and Molet 2010). Closer to the origin of eusociality, however, in so-called primitively eusocial taxa, there may primarily be small or even zero size differences (Field and Foster 1999;Field et al 2010;Kapheim et al 2012;Pennell and Field 2021). It is plasticity in the face of these developmental effects that we focus on in this paper.…”

“…Multiple paternity and unrelated alien workers are both found in primitively eusocial taxa (e.g. Pennell and Field 2021), altering worker-brood relatedness. However, these differences may be too subtle for workers to detect (Soro et al 2011) and the obvious change in size between the foundress and replacement queen may provide a better cue.…”

“…Reproductives may strategically produce lower quality worker offspring in order to reduce queen-worker conflict and place offspring in a position where helping is their best option (Brand and Chapuisat 2012;Kapheim et al 2015;Couchoux and Field 2019). In our study species, the primitively eusocial sweat bee Lasioglossum malachurum (Hymenoptera: Apoidea, Halictidae), the original queen dies before the end of the season in approximately one-third of nests (Pennell and Field 2021). Hence, from the viewpoint of the reproductive, there may be a trade-off between producing a socially controllable worker versus a successful future reproductive.…”