Environmental and genetic components of a major evolutionary transition: social plasticity in halictine bees.

Lead Research Organisation: University of Sussex
Department Name: Sch of Life Sciences

Abstract

The evolution of sociality is one of the major transitions in evolutionary biology. The key testing ground for theories concerning the origin of helping have been primitively eusocial taxa, in which behaviour is highly plastic. Social phenotype varies within these species, both temporally and spatially, from non-social to fully eusocial. Differences in social phenotype are correlated with factors such as latitude, altitude and habitat features. Yet the extent to which differences are genetically based, or represent condition-sensitive phenotypic expression, is almost unknown. Our research will use a combination of large-scale manipulative field experiments and molecular genetic analyses: (1) To test whether inter-population variation in social phenotype represents genetic differentiation or is a phenotypic response to environmental conditions. (2) To investigate the transition between social phenotypes along an environmental gradient. (3) To quantify the degree of reproductive isolation between the two social forms at a transition zone between them. (4) To test whether social populations form a grouping distinct from non-social populations in an intraspecific phylogeny. The work will involve a collaboration between researchers at University College London and Queen's University Belfast, employing a postdoctoral researcher and a 75% time technician. The study system will be British populations of sweat bees.

Related Projects

Project Reference Relationship Related To Start End Award Value
NE/C520439/1 01/02/2006 31/08/2007 £207,183
NE/C520439/2 Transfer NE/C520439/1 01/09/2007 31/12/2009 £111,845
 
Description The origin of sociality has been identified as one of the major transitions in evolution, yet the proximate mechanisms underlying it are poorly understood. In socially polymorphic taxa such as our study system, the sweat bee Halictus rubicundus, individuals in some populations form social groups while those in other populations are non-social. This provides a unique opportunity to understand the genetic and environmental influences involved in the transition without the complication of interspecific differences.

The critical objective in the proposal was to determine the extent to which differences between populations in social phenotype represent genetic differences or plasticity. Through careful monitoring of sites across the UK and Ireland, we found that populations in northern/high altitude sites were non-social, whereas populations in southern low altitude sites were social. Large-scale field transplants then showed unambiguously that these differences largely represent plasticity. H. rubicundus foundresses from northern sites produced social nests when transplanted to southern sites. Microsatellite genotyping of offspring and potential mothers showed that these nests indeed exhibited the hallmark of sociality: high reproductive skew with a division of labour between foragers and a non-foraging reproductive. Our findings show that sociality remains a functional phenotype in northern bees, despite not being exposed to selection there for >200 years (based on historical weather data). Reverse transplants produced similar results: foundresses from social populations all had non-social nests at sites where natives are non-social. Furthermore, there was little evidence of differences between bees from different sources when placed in a common garden, in terms of traits less directly linked to sociality, such as foraging success and nest initiation date. Social phenotypes expressed by transplanted bees were not affected by whether the bees experienced the winter at their natal (pre-transplant) or post-transplant sites. Bees transplanted to the south were more likely to have social nests if (1) offspring production was initiated earlier in Spring, consistent with the prediction that sociality is promoted by a longer growing season; and (2) if the foundress was still alive when her offspring reached adulthood, a pattern predicted on both genetic and ecological grounds.

The origin of sociality is often regarded as a change of macroevolutionary proportions. Yet a general conclusion from our findings is that switches between sociality and non-sociality have probably occurred frequently and instantaneously during sweat bee evolution in response to environmental change, via expression of pre-existing integrated but cryptic phenotypes rather than requiring convergent evolution. Rapid switching has probably allowed halictines to invade new biogeographic regions, and could enable bee pollinators to more easily accommodate the global warming that is currently predicted. Indeed, the simultaneous origin of sociality in halictine lineages is linked with past episodes of warming. Subsequent adaptation may have involved loss of plasticity in some taxa, probably including North American populations of H. rubicundus, which can be socially more complex than the populations we studied.

A second objective was to determine whether populations expressing different social phenotypes are reproductively isolated. Sequencing of mitochondrial DNA and use of microsatellites developed specifically for this study revealed genetic differentiation correlated with the geographic distance between populations, independent of their social phenotype. This indicates that the two social forms are not reproductively isolated. It contrasts with studies of US H. rubicundus, where there is significant mitochondrial differentiation between populations expressing the two phenotypes.

A third objective was to identify climatic correlates of social phenotype and examine possible cues used by bees when deciding how to behave. Across sites, sociality was correlated with higher spring temperatures and hence longer growing seasons. However, unlike many other insects that must choose whether to enter hibernation or reproduce in the current year, we found that decision-making in H. rubicundus does not depend only on photoperiod. A previous study in the US suggested a complex mechanism where sex-ratios interact with mating latency to determine individual behaviour. A model we have developed indicates that this strategy is evolutionary stable only under restrictive conditions.
Exploitation Route This research is primarily of interest to other academics in fields such as evolutionary biology and animal behaviour, but it could also be of interest to those studying how climate change may affect pollination services. This research is primarily of interest to other academics in fields such as evolutionary biology and animal behaviour, but it could also be of interest to those studying how climate change may affect pollination services.
Sectors Environment

 
Description Academic advance The origin of sociality has been identified as one of the major transitions in evolution, yet the proximate mechanisms underlying it are poorly understood. Socially polymorphic taxa such as our study system, in which individuals in some populations form social groups while those in other populations are non-social, provide a unique opportunity to understand the genetic and environmental influences involved in the transition to sociality without the complication of interspecific differences. The origin of sociality is often regarded as a change of macroevolutionary proportions. Yet a general conclusion from our findings is that switches between sociality and non-sociality have probably occurred frequently and instantaneously during sweat bee evolution in response to environmental change, via expression of pre-existing integrated but cryptic phenotypes rather than requiring convergent evolution. Rapid switching has probably allowed halictines to invade new biogeographic regions, and could enable bee pollinators to more easily accommodate the global warming that is currently predicted.
First Year Of Impact 2010
Sector Environment
Impact Types Cultural

 
Description DEL PhD studentship scheme
Amount £36,000 (GBP)
Organisation Government of Northern Ireland 
Department Department for Employment and Learning Northern Ireland (DELNI)
Sector Public
Country United Kingdom
Start 10/2008 
End 09/2011
 
Description ERC Advanced Grant
Amount € 2,400,000 (EUR)
Funding ID 695744 
Organisation European Research Council (ERC) 
Sector Public
Country European Union (EU)
Start 01/2017 
End 12/2021
 
Description Joint-funded: 50% NERC studentship (quota)/50% Sussex University
Amount £35,409 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 01/2012 
End 07/2015
 
Description Caste determination through mating in primitively eusocial societies 
Organisation University of Lausanne
Country Switzerland 
Sector Academic/University 
PI Contribution Collaboration bringing together the theoretical and empirical knowledge of the different contributors
Collaborator Contribution Mathematical modelling
Impact LUCAS, E.R. & FIELD, J. (2013). Caste determination through mating in primitively eusocial societies Journal of Theoretical Biology 335:31-39
Start Year 2010
 
Description Environmental and genetic components of a major evolutionary transition 
Organisation Martin Luther University of Halle-Wittenberg
Country Germany 
Sector Academic/University 
PI Contribution Collaboration bringing together expertise from evolutionary biology and molecular ecology
Collaborator Contribution Research ideas
Impact Conference contribution
Start Year 2010
 
Description Sex-biased dispersal, haplodiploidy and the evolution of helping in social insects 
Organisation University of Cambridge
Country United Kingdom 
Sector Academic/University 
PI Contribution Collaboration bringing together the theoretical and empirical knowledge of the different contributors
Collaborator Contribution Mathematical modelling, ideas
Impact JOHNSTONE, R.A., CANT, M.A. & FIELD, J. (2012). Sex-biased dispersal, haplodiploidy and the evolution of helping in social insects. Proceedings of the Royal Society of London Series B 279:787-793
Start Year 2007