PERSPECTIVE PERSPECTIVE Natural selection drives the evolution of ant life cycles Edward O. Wilsona,1 and Martin A. Nowakb aMuseum of Comparative Zoology, Harvard University, Cambridge, MA 02138; and bProgram for Evolutionary Dynamics, Department of Organismic and Evolutionary Biology, and Department of Mathematics, Harvard University, Cambridge, MA 02138 Contributed by Edward O. Wilson, June 9, 2014 (sent for review December 17, 2013) The genetic origin of advanced social organization has long been one of the outstanding problems of evolutionary biology. Here we present an analysis of the major steps in ant evolution, based for the first time, to our knowledge, on combined recent advances in paleontology, phylogeny, and the study of contemporary life histories. We provide evidence of the causal forces of natural selection shaping several key phenomena: (i) the relative lateness and rarity in geological time of the emergence of eusociality in ants and other animal phylads; (ii) the prevalence of monogamy at the time of evolutionary origin; and (iii) the female-biased sex allocation observed in many ant species. We argue that a clear understanding of the evolution of social insects can emerge if, in addition to relatedness-based arguments, we take into account key factors of natural history and study how natural selection acts on alleles that modify social behavior. sociobiology | claustrality | adaptive radiation | inadequacy of inclusive fitness Comparative studies have revealed that from in the primitive termite species Zootermopsis insects, especially ants, leading to super- the moment of the evolutionary origin of nevadensis. During encounters of two adja- organisms (10–14). However, in almost all animal eusociality, which is at first facultative cent unrelated colonies nesting under bark, cases precise models of social interactions in nature, each worker is in a tug-of-war be- the single or multiple queens and kings of and evolutionary dynamics have not been tween it and the colony of which it is a part. one of the Zootermopsis colonies are killed formulated but instead have been replaced As colony-level selection becomes more im- in combat, and their surviving offspring by arguments based on imaginary inclusive portant, however, individual survival and re- merge into one colony. Members of both col- fitness concepts, which are not grounded in production become less important to the onies then cooperate as a single unit. Replace- a mathematical description of evolution. worker’s personal genetic fitness, and the sur- ment reproductives develop from helpers of Here we approach the issue in a novel man- vival and reproduction of the colony become both original colonies and may interbreed (8). ner, from geological history, phylogeny, and more so. Finally, in obligatory eusociality, the Competition between colonies of the same the details of comparative colony life cycles. capacity for worker reproduction within the ant species does not consist exclusively of genome ceases, creating the ultimate insect overt combat and predation by large colonies The Geological Origins of Eusociality superorganism (1, 2). Ultimate superorgan- on small colonies of the same species. It also Although theory must be built upon facts, isms,inwhichthefemaleworkerslackany includes competition through the preemp- factual information makes little sense unless capacity to reproduce, are found in doryline tion of nest and foraging sites as well as woventogetherasevolutionaryhistory.Within army ants, Atta fungus growers, and the ant superiority in harvesting nest materials and biology, this principle is illustrated by every genera Solenopsis, Pheidole, Monomorium, food. Theoretical and experimental studies aspect of social evolution. Tetramorium,andLinepithema.Workersin combined have demonstrated that all these In tracking the historic origins of euso- the last five genera lack ovaries altogether. On colony-level endeavors depend primarily on ciality, we recognize that eusociality is a rare the other hand, in a few clades of species the colony size, a genetically determined group- and relatively late arrival in the very long capacity of workers to reproduce has returned level phenotype, as displayed in monogyne- evolution of insects as a whole. It was the last or at least has been augmented by second- versus-polygyne strains of many ant species of the great evolutionary advances through ary evolution, allowing individual workers (2, 6) and thought to precede the distinction geological time, following (in chronological to assume the role of queen (3, 4). At the of closely related species (2, 6). The number order) winged flight, the folding of wings extreme superorganismic phase, the level of of participating workers alone has a profound over the back, and complete metamorphosis. selection becomes the genome of the queen effect on the colony’s metabolic growth rate, It arose only after repeated diversifications and the sperm she stores, and the workers life cycle, reproductive allocation, and mature of the insects and other hexapods across 325 can be viewed as the robotic extensions of size. The relationships mirror the metabolic million years. her phenotype (5). scaling laws for mass and physiology of in- The oldest known parainsectans, compris- Conflict between colonies may arise by dividual organisms (9). Mathematical model- ing neanurid (15) and isotomid collembolans direct physical contact, resulting either in ing suggests that the critical demographic retreat or complete destruction (“myrmi- factor in the competitive growth of insect ” Author contributions: E.O.W. performed research; M.A.N. analyzed cide ) of the losing colony. Examples that colonies is the initial fecundity and expected data; and E.O.W. and M.A.N. wrote the paper. have been well studied include fire ants of life-time of the founding queen (5). The authors declare no conflict of interest. the genus Solenopsis (6), weaver ants (Oeco- A popular testing ground of inclusive Freely available online through the PNAS open access option. phylla), and honeypot ants (Myrmecosystus) fitness theory has been the colony life cycles 1To whom correspondence should be addressed. Email: ewilson@ (7). Comparable programmed warfare occurs and within-colony behavior of eusocial oeb.harvard.edu. www.pnas.org/cgi/doi/10.1073/pnas.1405550111 PNAS | September 2, 2014 | vol. 111 | no. 35 | 12585–12590 Downloaded by guest on September 28, 2021 (16),datetotheEarlyDevonian(419–393 of an anatomically distinct worker caste, the The Approach of and Breakthrough to Mya). The earliest fossil, a pterygote insect at hallmark of obligatory eusociality (26–33). Eusociality ca.415Mya,isRhyniognatha hirsti (17). It is This evidence, albeit negative, deserves at- Whywaseusocialitysolateincoming,and not the most basal, however; other evidence tention because of its relevance to the general why has it remained so rare, when it has points to the primitively wingless Archae- theory of eusocial evolution. It supports the proven so ecologically successful? Numerous ognatha in that role (18). It is very likely that conclusion that eusociality—or at least its candidate phylads and environmental op- the earliest insects had a common ancestor advanced, obligatory level—has been rare portunities to advance into eusociality have that appeared bristletail-like (18) but actually and came late in geological time. Additional been present on the land as well as in the would not have been part of the crown-group support for this perception comes from the fresh and shallow marine waters since the Archaeognatha. The Paleozoic evolution of first terrestrial invasion by multicellular life. the insects, paralleling that of the vertebrates continued sparseness of the origination of eusociality in the Mesozoic and Cenozoic At least tens of thousands, more likely hun- and other invertebrates, then passed through dreds of thousands, of insect species were Eras. The number of known events that two successive phases. The first, lasting until present and diversifying during the late Pa- created obligatory eusociality in contempo- the start of the Late Carboniferous (about 323 leozoic and early Mesozoic Periods, during raryanimalsasawholeisonly18:threein Mya), was characterized by a scarcity of fos- which they occupied a wide range of niches. sils and potentially limited biodiversity (19). synalpheid shrimps; two in the vespid wasps, The Pennsylvanian tree fern Psaronius,for The second phase was a major adaptive ra- scolytid beetles, and bathergid mole-rats; and – example, was host to at least seven insect diation during the Early Late Carboniferous one each in ants, termites, sphecid wasps, groups with different feeding habits, in- boundary, resulting in the origin of winged allodapine bees, augochlorine bees, corbicu- cluding external foliage consumption, insects and an abundance of new insect late bees, halictine bees, thrips, and aphids piercing and sucking, stem boring, galling, orders (20) including the appearance of the (22, 34). A cockroach species (Sociala perlu- spore consumption, and ingesting litter and most advanced major lineage of insects, the cida) from the Early Cretaceous has been peat at the base of the tree (33). Many types Holometabola characterized by an egg-larva- interpreted as being eusocial from a single of life cycles and dispersal mechanisms pupa-adult development (21). By the late specimen (35), but the claim needs additional have existed from that time onward. Also, Paleozoic Era, the fauna had begun to acquire various