Extreme and Variable Climatic Conditions Drive the Evolution of Sociality in Australian Rodents.

Climate change is generating an intensification of extreme environmental conditions, including frequent and severe droughts [1] that have been associated with increased social conflict in vertebrates [2-4], including humans [5]. Yet, fluctuating climatic conditions have been shown to also promote cooperative behavior and the formation of vertebrate societies over both ecological and evolutionary timescales [6]. Determining when climatic uncertainty breeds social discord or promotes cooperative living (or both) is fundamental to predicting how species will respond to anthropogenic climate change. In light of this, our limited understanding of the order of evolutionary events-that is, whether harsh environments drive the evolution of sociality [6] or, alternatively, whether sociality facilitates the invasion of harsh environments [7]-and of how cooperation and conflict coevolve in response to environmental fluctuation represent critical gaps in knowledge. Here, we perform comparative phylogenetic analyses on Australian rodents (Muridae: Hydromyini) and show that sociality evolves only under harsh conditions of low rainfall and high temperature variability and never under relatively benign conditions. Further, we demonstrate that the requirement to cooperate under harsh climatic conditions generates social competition for reproduction within groups (reflected in the degree of sexual dimorphism in traits associated with intrasexual competition [8]), which in turn shapes the evolution of body size dimorphism. Our findings suggest that as the environment becomes more severe [1], the resilience of some species may hinge on their propensity to live socially, but in so doing, this is likely to affect the evolution of traits that mediate social conflict.

Protein-Level Interactions as Mediators of Sexual Conflict in Ants.

All social insects with obligate reproductive division of labor evolved from strictly monogamous ancestors, but multiple queen-mating (polyandry) arose de novo, in several evolutionarily derived lineages. Polyandrous ant queens are inseminated soon after hatching and store sperm mixtures for a potential reproductive life of decades. However, they cannot re-mate later in life and are thus expected to control the loss of viable sperm because their lifetime reproductive success is ultimately sperm limited. In the leaf-cutting ant Atta colombica,, the survival of newly inseminated sperm is known to be compromised by seminal fluid of rival males and to be protected by secretions of the queen sperm storage organ (spermatheca). Here we investigate the main protein-level interactions that appear to mediate sperm competition dynamics and sperm preservation. We conducted an artificial insemination experiment and DIGE-based proteomics to identify proteomic changes when seminal fluid is exposed to spermathecal fluid followed by a mass spectrometry analysis of both secretions that allowed us to identify the sex-specific origins of the proteins that had changed in abundance. We found that spermathecal fluid targets only seven (2%) of the identified seminal fluid proteins for degradation, including two proteolytic serine proteases, a SERPIN inhibitor, and a semen-liquefying acid phosphatase. In vitro, and in vivo, experiments provided further confirmation that these proteins are key molecules mediating sexual conflict over sperm competition and viability preservation during sperm storage. In vitro, exposure to spermathecal fluid reduced the capacity of seminal fluid to compromise survival of rival sperm in a matter of hours and biochemical inhibition of these seminal fluid proteins largely eliminated that adverse effect. Our findings indicate that A. colombica, queens are in control of sperm competition and sperm storage, a capacity that has not been documented in other animals but is predicted to have independently evolved in other polyandrous social insects.