Building a new research framework for social evolution: intralocus caste antagonism

Abstract

The breeding and non-breeding ‘castes’ of eusocial insects provide a striking example of role-specific selection, where each caste maximises fitness through different morphological, behavioural and physiological trait values. Typically, queens are long-lived egg-layers, while workers are short-lived, largely sterile foragers. Remarkably, the two castes are nevertheless produced by the same genome. The existence of inter-caste genetic correlations is a neglected consequence of this shared genome, potentially hindering the evolution of caste dimorphism: alleles that increase the productivity of queens may decrease the productivity of workers and vice versa, such that each caste is prevented from reaching optimal trait values. A likely consequence of this ‘intralocus caste antagonism’ should be the maintenance of genetic variation for fitness and maladaptation within castes (termed ‘caste load’), analogous to the result of intralocus sexual antagonism. The aim of this review is to create a research framework for understanding caste antagonism, drawing in part upon conceptual similarities with sexual antagonism. By reviewing both the social insect and sexual antagonism literature, we highlight the current empirical evidence for caste antagonism, discuss social systems of interest, how antagonism might be resolved, and challenges for future research. We also introduce the idea that sexual and caste antagonism could interact, creating a three-way antagonism over gene expression. This includes unpacking the implications of haplodiploidy for the outcome of this complex interaction.

Phenotypic correlation between queen and worker brood care supports the role of maternal care in the evolution of eusociality

“…The degree of overlap is expected to be highest in facultatively and primitively eusocial species, where there is little to no queen–worker dimorphism and maternal and sibling care behaviors are phenotypically identical. The overlap is predicted to be lowest in obligately eusocial species with strong queen–worker dimorphism (although caste antagonism, antagonistic selection between castes, likely prevents either caste from expressing its optimal caste‐specific phenotype; Linksvayer & Wade, ; Pennell et al., ). Transcriptomic studies in primitively eusocial vespid wasps, bumble bees, and facultatively eusocial carpenter bees that explored the overlap of transcriptome‐wide gene expression profiles between workers and queens engaged in maternal care provide preliminary support for these predictions (Rehan, Berens, & Toth, ; Toth et al., , ; Woodard, Bloch, Band, & Robinson, ).…”

“…Here, we estimated the phenotypic correlation between queen and worker care behaviors in the black garden ant Lasius niger , as a first exploration of the quantitative genetic predictions of the maternal heterochrony hypothesis and also to test whether we find evidence for intercaste correlations for brood care, as predicted by the intralocus caste antagonism framework (Pennell et al., ). In many ant species including L .…”

“…Based on the maternal heterochrony hypothesis and hypotheses regarding the evolution of intercaste correlations (Holman, ; Holman et al., ; Linksvayer & Wade, ; Pennell et al., ), we make the following predictions: (a) If queen and worker nursing behaviors are genetically correlated due to pleiotropy, queen and worker nursing behaviors should also be phenotypically correlated; (b) If our measure of brood care is tied to colony fitness, we expect to find a positive relationship between brood care and colony productivity. We tested these predictions by measuring colony productivity and the nursing behavior of L .…”

“…Therefore, queen-and worker-expressed care behaviors are predicted to be genetically and phenotypically correlated to some degree (Linksvayer & Wade, 2005). Such intercaste genetic correlations are expected to broadly affect the evolution of queen and worker traits, and may constrain the independent optimization of queen and worker traits (Holman, 2014;Holman, Linksvayer, & d'Ettorre, 2013;Pennell, Holman, Morrow, & Field, 2018).…”

“…Here, we estimated the phenotypic correlation between queen and worker care behaviors in the black garden ant Lasius niger, as a first exploration of the quantitative genetic predictions of the maternal heterochrony hypothesis and also to test whether we find evidence for intercaste correlations for brood care, as predicted by the intralocus caste antagonism framework (Pennell et al, 2018). In many ant species including L. niger, after mating, a single queen excavates a chamber, seals herself in, lays a first clutch of eggs, and independently cares for this first batch of larvae using fat reserves and wing musculature (Keller & Passera, 1989;Sommer & Holldobler, 1995).…”