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The Endocrinology and Evolution of Tropical Social Wasps: from Casteless Groups to High Societies

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The Endocrinology and Evolution of Tropical Social Wasps: from Casteless Groups to High Societies 1 The endocrinology and evolution of tropical social wasps: from casteless groups to high societies Hans Kelstrup A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy University of Washington 2012 Reading Committee: Lynn M. Riddiford, Chair James W. Truman Jeff Riffell Program Authorized to Offer Degree: Biology Department 2 ©Copyright 2012 Hans Kelstrup 3 University of Washington Abstract The endocrinology and evolution of tropical social wasps: from casteless groups to high societies Hans Kelstrup Chair of the Supervisory Committee: Dr. Lynn M. Riddiford Biology Department The endocrinology and behavior of three social vespid wasps was studied in northeast Brazil (São Cristóvão, Sergipe) from 2010-2011. There were two main objectives of this work: to test a hypothesis on the origin of reproductive castes (i.e. queen and worker phenotypes) in a communal species (Zethus miniatus: Eumeninae), and to describe the endocrinology of two highly eusocial swarm founding species (Polybia micans and Synoeca surinama: Polistinae). Wasps offer an unparalleled opportunity for research on social evolution due to the continuous range of social organization among extant species. Yet little work has been devoted to the study of wasp physiology beyond Polistes, a large genus of primitively eusocial paper wasps. In Polistes, juvenile hormone (JH) has been shown to be important for reproduction, dominance, chemical signaling (e.g., cuticular hydrocarbons (CHCs)) in queens while promoting the early onset of certain tasks in workers. Evidence for a similar mechanism in bees and ants suggests a dual function of JH was intact in the last common ancestor of these groups (the sting- 4 possessing Hymenoptera). The ancestor was undoubtedly a wasp; since eusocial hymenopterans feed helpless brood as they grow, it is likely that the ancestor was also a progressive provisioner, a rare behavior in solitary wasps and bees. The emergence of prolonged maternal care may have set the stage for caste-like phenotypes to arise: an aggressive egg-laying phase (queen-like) followed by an alleged ovary-reduced phase associated with the brood rearing (worker-like). I tested this hypothesis in Z. miniatus, a progressive provisioning, group-living wasp with behavioral traits reminiscent of her caste- containing relatives, such as the susceptibility to adopt a hungry larva. Ironically, the high frequency of another behavior characteristic in eusocial societies, the destruction of nestmate eggs, appears to undermine the hypothesis on caste origin: the high rates of brood killing observed in nests of Z. miniatus likely explain why females produce multiple eggs at a time (i.e. there is not pronounced ovarian cycle). JH titers did not differ between gravid females looking for a cell (potential brood killers) and provisioners of young larvae. Instead, JH titers were high on a nest where females outnumbered cells, but once cells came to outnumber females, JH levels dropped precipitously, suggesting JH has a role in social competition, a relationship observed in Polistes. These results led me to expect a role for JH in reproductive competition in the swarm founders, where multiple, contending queens are the norm. Surprisingly, despite the similarity in the social structure between P. micans and S. surinama, in which both species determine caste in the adult stage, the endocrine profile of these two wasps could hardly be more different. For instance, queens of S. surinama had elevated titers compared to workers whereas JH titers were indistinguishable between queens and workers in oligarchic nests of P. micans. In complete contrast to the pattern observed in Polistes, only lone queens (lacking direct competition) of P. micans had elevated JH in non-swarming nests. JH titers did spike, however, in potential reproductives who were on a nest without a queen. Within a day or two, JH levels plummeted in these prospective replacement queens as they began producing eggs. In S. surinama, the rise in JH followed behavioral displays of dominance and remained high, 5 shaping a queen-like CHC profile and likely functioning as a gonadotropin. When these swarm founders shared a pattern in their endocrine profile, they typically contrasted with that observed in Polistes. For instance, circulating ecdysteroids are important for establishing dominance in Polistes, yet they are not biologically relevant in P. micans or S. surinama. The wild deviations in endocrine function in these wasps parallel the loss (or inversion) of hormone functions seen in highly derived bees and queenless ants. Fortunately, in the case of wasps, there is promise to track how hormone function was modified through evolution thanks to the preservation of wide-ranging social (and pre-social) arrangements present in today’s wasps. 6 The endocrinology and evolution of tropical social wasps: from casteless groups to high societies Chapter 1 (pp. 7-44) A brief review of social insect endocrinology with an emphasis on the Hymenoptera Chapter 2 (pp. 45-72) The endocrinology and behavior of Zethus miniatus Chapter 3 (pp.73-125) The endocrinology of Polybia micans Chapter 4 (pp. 126-178) The endocrinology of Synoeca surinama 7 Chapter 1: A brief review of social insect endocrinology with an emphasis on the Hymenoptera Table of Contents Introduction ................................................................................................................................................... 8 Juvenile hormones and the ecdysteroids: development and reproduction .................................................... 9 Termites ...................................................................................................................................................... 11 The Hymenoptera ........................................................................................................................................ 14 Caste determination: Development ......................................................................................................... 15 Bees ..................................................................................................................................................... 16 Wasps .................................................................................................................................................. 18 Ants ..................................................................................................................................................... 21 Endocrine Regulation of Reproduction and Dominance ........................................................................ 22 Primitively eusocial bees .................................................................................................................... 22 Primitively eusocial wasps .................................................................................................................. 25 Derived eusocial Hymenoptera ........................................................................................................... 28 Endocrine Regulation of Worker Behavior ............................................................................................ 30 Major gaps in our understanding of social evolution .................................................................................. 32 References ................................................................................................................................................... 35 8 Introduction The evolution of insect societies has fascinated and challenged biologists ever since Charles Darwin first tried to accommodate for neuter castes in his theory of natural selection (Darwin, 1859). Indeed, sterile workers have attracted much attention over the century for reasons on why they forego their own reproduction and help raise another’s offspring (Wilson, 1971). The only satisfying explanations to date for the existence of workers are kin selection (Hamilton, 1964a, b), mutualism (West-Eberhard, 1978b) and/or other hypotheses relating to self-interest (e.g., nest-inheritance opportunities among co-nesting non-relatives (Leadbeater et al., 2011)). The resurgence of group selection proponents (Nowak et al., 2010; Wilson and Wilson, 2008), who claim kin selection is inconsequential for the evolution of workers, promises to reignite a debate thought settled decades ago. Whatever consensus is reached on the ultimate reasons for caste evolution, there looms an arguably more important question that addresses the origins of macroevolutionary change: how, mechanistically, did castes originate? And once the reproductive castes were established, how were worker and queen phenotypes fine-tuned for a more efficient division of labor? Worker phenotypes have evolved many times over, from minute sponge-dwelling shrimp (Duffy, 1996) to naked mole rates (O'Riain et al., 2000), but the most well-known examples come from the insects (Wilson, 1971). The ants, honeybees and termites are famous for their amazing emergent complexity and morphologically discrete queens and workers. Except for a handful of highly derived species which employ genetic mechanisms for determining caste (Evison and Hughes, 2011; Hartfelder et al., 2006), to study caste differentiation is to study developmental plasticity, where multiple phenotypes (physiologies, behaviors and morphologies) can be generated from the same genotype. In insects, mechanisms of caste differentiation (and environmental-triggered
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