The Termite Worker Phenotype Evolved as a Dispersal Strategy for Fertile Wingless Individuals before Eusociality Thomas Bourguignon, 1,2, * Ryan A. Chisholm, 1 and Theodore A. Evans 1,† 1. Department of Biological Sciences, National University of Singapore, Singapore 117591; 2. Czech University of Life Sciences, Faculty of Forestry and Wood Sciences, Prague, Czech Republic Submitted March 20, 2015; Accepted September 10, 2015; Electronically published January 20, 2016 Online enhancements: appendixes. abstract: Termites are eusocial insects that evolved from solitary cockroaches. It is not known precisely what factors drove the evolu- tion of termite eusociality, that is, skewed reproduction with distinct winged reproductive and wingless worker phenotypes. In other eu- social insects (bees and wasps), reproductive skew evolved first and phenotype differences evolved second. We propose that the reverse pattern occurred in termites, that is, that the winged-wingless di- phenism evolved before eusociality. We discuss existing phylogenetic and pheromonal evidence supporting our hypothesis. We provide new experimental evidence from the most basal termite species (Mastotermes darwiniensis), suggesting that the ancestral state was indeed diphenic but presocial. We propose that the mechanism promoting a winged-wingless diphenism—in the absence of eusociality—was greater predation of ae- rial than terrestrial dispersers, and we support this with a game theoretic model. We augment our hypothesis with a novel explanation for the evo- lution of the developmental pathways leading to winged and wingless phenotypes in termites. An added benefit of our hypothesis is that it neatly explains the origin of termite eusociality itself: in the pre-eusocial ancestral species, the poor dispersal ability of the wingless phenotype would have led to clustering of relatives around shared resources—a pre- requisite for nonparental care of close relatives. Keywords: castes, Isoptera, Mastotermes, phenotype, reproductive skew, social behavior. Introduction In many animal species, some individuals forgo their own (direct) reproduction to help raise the young of others, a phenomenon called eusociality (following Michener 1969; Wilson 1971; Sherman et al. 1995). The evolutionary driv- ing force behind this apparent altruism is believed to be kin selection, whereby the nonreproductives gain inclusive (indi- rect) fitness by helping their relatives reproduce (Hamilton 1963, 1964a, 1964b; Maynard Smith 1964; Bartz 1979; An- dersson 1984). The most extreme examples of this reproduc- tive skew (also called reproductive division of labor) have evolved in the eusocial insects, which include all ants, some bees and some wasps (order Hymenoptera), and all termites (which are social cockroaches; order Blattodea, epifamily Isoptera; Lo et al. 2000; Inward et al. 2007a). Eusocial insect species typically have distinct phenotypes called castes, which are adapted to perform specialized roles (Oster and Wilson 1979; Simpson et al. 2011). In the simplest case, there are two castes: reproductives, usually called queens and kings, and nonreproductives or steriles, usually called workers (for a list of names, see table 1). Studies on bees and wasps show that in these taxa, the worker phenotype evolved after eusociality as a response to the specialized tasks performed by reproductive and nonreproductive individuals. Social insect species with skewed reproduction but without a phenotypically distinct worker caste are considered primitively eusocial, whereas those with one are considered highly eusocial (fig. 1). This distinction between primitively and highly eusocial was first made for bees (Michener 1974) and adapted for wasps (O’Donnell 1998). These eusocial categories are supported by correspondence with the phylogenies of the social spe- cies in bees (Danforth 2002) and wasps (Pilgrim et al. 2008). The main phenotypic differences between queens and workers in bees and wasps are in genitalia (reduced in workers) and size (workers are smaller). All individuals in these taxa have wings: queens disperse and workers for- age through the air. Although the evolution of eusociality first—followed by phenotypically distinct workers (i.e., castes) evolving sec- ond—is well accepted for bees and wasps, there is no con- sensus on whether this holds true for termites (where eusociality evolved independently). This is because the phylogenetic pattern of reproductive behavior from sol- * Present address: School of Biological Sciences, University of Sydney, Sydney, New South Wales 2006, Australia. † Corresponding author. Present address: School of Animal Biology, Univer- sity of Western Australia, Perth, Western Australia 6009, Australia; e-mail: cryptotermes@gmail.com. Am. Nat. 2016. Vol. 187, pp. 000–000. q 2016 by The University of Chicago. 0003-0147/2016/18703-56151$15.00. All rights reserved. DOI: 10.1086/684838 vol. 187, no. 3 the american naturalist march 2016 This content downloaded from 130.095.088.064 on January 20, 2016 18:58:18 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).