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Home , Formica exsecta, Gigantopterid, Microstigmus, Progressive provisioning, Sociala

PERSPECTIVE PERSPECTIVE Natural selection drives the of 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 in and other phylads; (ii) the prevalence of monogamy at the time of evolutionary origin; and (iii) the female-biased sex allocation observed in many ant . We argue that a clear understanding of the evolution of social 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.

| claustrality | adaptive radiation | inadequacy of inclusive fitness

Comparative studies have revealed that from in the primitive 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 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 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 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 , 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 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 (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 , The Pennsylvanian tree 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, , sphecid wasps, groups with different feeding habits, in- boundary, resulting in the origin of winged allodapine , augochlorine bees, corbicu- cluding external foliage consumption, insects and an abundance of new insect late bees, halictine bees, thrips, and piercing and sucking, stem boring, galling, orders (20) including the appearance of the (22, 34). A species (Sociala perlu- spore consumption, and ingesting litter and most advanced major lineage of insects, the cida) from the Early has been peat at the base of the tree (33). Many types Holometabola characterized by an egg-- 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 degrees of relatedness, from clonal a strong modern cast, although the main part evidence. On the other hand, a more im- to unrelated, probably were present in of the process was ushered in by the mass mediately plausible case might be made for groups of individuals, as they are today in extinction at the end of the Period. including human beings, because of the ex- modern lineages of Paleozoic origin. Ofthe28insectordersalivetoday(the istence of the postmenopausal “caste” of At the present time social aggregations of number recognized varies slightly according grandmother helpers (36). ancient origin, still short of eusociality, occur to taxonomic opinion), 14 were present at Other examples, especially among arthro- in different patterns and degrees of com- that time. The Paleozoic survivors include pods, almost certainly will be found, but we plexity in a majority of the insect orders. many of our most familiar insects: barklice, doubt that the number ever will rise to more Massed offspring are tended by mothers and thrips, hemipterans such as treehoppers and than the tiny fraction of all the animal phy- sometimes fathers as well. In a few cases shield bugs, dobsonflies and other neurop- lads and of the species the phylads comprise. terans, mayflies, dragonflies, orthopterans, these offspring are led by their parents from For example, all the known species of ants, one place to another. According to species, , stoneflies, and beetles (especially termites, and eusocial bees and wasps make archostematans) (20, 22, 23). Of the 14 orders theyoungareeitherprotectedbynestsor up only about two percent of the nearly 1 known to have originated in the following kept in the open. For example, long-term million known insect species (2). Mesozoic Era, all are present today. care and protection of young has been ob- Theoriginsofthelivinginsecteusocial ThelatePaleozoicinsectsnotonlywere served in membracid treehoppers, scutellerid abundant, diverse, and relatively advanced lines were scattered across the Mesozoic and jewel bugs, belostomatid giant water bugs, anatomically (24) but also, as evidenced by Cenozoic Eras. Termites were the earliest gall-dwelling aphids, tingid lacebugs, praying the amount of fossil damage, constituted among them, projected to have evolved from , earwigs, and argid sawflies. Tight a major environmental force in the peat- cockroach-like ancestors during the Middle masses of larvae, adults, or both, in some accumulating forests and nearby better- to Early (237–174 Mya) (37). cases capable of organized movement, occur drained habitats that dominated the land. The eusocial corbiculate bees, particularly the in species as diverse as gyrinid whirligig By the end of the Permian Period, herbiv- bumble bees (tribe Bombini), honey bees beetles, psocopteran barklice, embiidine ory, called by Beck and Labandeira (25) (Apini), and stingless bees (Meliponini), evi- webspinners, noctuid and lasiocampid “the basic trophic machinery of insects,” dently originated variously toward the end of moths, acridid lubber grasshoppers, ten- reached one-third that in modern rain the Cretaceous Period, as far back as 87 Mya, thridinid and pamphilid sawflies, and cockroaches (38, 39). forests for one lineage of , and during the early Paleogene Period (27, From this evolving mélange of subsocial the gigantopterids. 28). The origin of eusociality in halictid bees Across the span of the second phase of insect and other animal species has arisen the occurred during the mid-Paleogene Period, Paleozoic evolution (323–252 Mya), the rich very small subset of independent lines of 35 Mya (27, 28). The ants appeared, evidently fossil record left no known evidence of living eusocial taxa. The key to their origin is eusocial insects. Some species might have from a single aculeate ancestor (29), that all these lines, with no known exception, existed in sparse populations, as exemplified during the Cretaceous Period, about 140 Mya first attained the same relatively rare pre- – today by modern Microstigmus wasps, or (29 31). By the Paleogene Period and likely adaptation comprising progressive care of the have lived in hidden niches, as do present- during the very Late Cretaceous, most or all young until maturity, by regular feeding or day scolytid beetles and gall-forming thrips. of the contemporary 21 ant subfamilies had inspection or both combined with protection As yet, however, no trace has been detected separated (29–31). against conspecific competitors and other

12586 | www.pnas.org/cgi/doi/10.1073/pnas.1405550111 Wilson and Nowak Downloaded by guest on September 28, 2021 enemies (34). The rearing of multiple larvae of insect colonies vary in their responses to few as five percent of the queens succeed in PERSPECTIVE by such progressive care in protected nests different tasks. When two or more individ- building a nest (51). Similar mortality rates has been of special importance as a presocial uals interact, the individuals with the lowest have been observed in the mating swarms of adaptation in the (36, 38, 40– thresholds for each localized task are the first other ant species with large mature colonies, 42). From nest construction and progressive to undertake it. The activity of the initiators including representatives of the genera Atta, care, only one short step is needed to achieve inhibits their colony-mates, who then are Pheidole,andPogonomyrmex (2, 52). eusociality, namely the silencing, by as little more likely to move on to whatever tasks Continuing this first explanation of the as a single mutation, of the propensity of the remain available (48, 49). monogamy window principle, it is likely, al- mother and offspring to disperse (34). though difficult to demonstrate, that high The ultimate cause of the critical pre- Monogamy and Origin of Eusociality rates of mortality also exist for dispersing adaptation (progressive care of offspring in A closely linked circumstance in early euso- queens of primitively eusocial species, even “ a protected nest) remains open to specula- cial evolution is the monogamy window though the starting numbers are much ” tion. The cause may have been nothing more hypothesis (50). The generalization is well smaller. Such is demonstrably the fate of than the advantage conferred by the posses- enough documented to be called a principle: facultatively eusocial wasps. Among 19 spe- sion of a residence, providing parents and All currently available evidence indicates cies studied, 38–100% of the nests con- offspring with a protected site from which that obligatory sterile eusocial castes arose structed by lone foundresses, who then were they could forage and to which they could only via the lifetime association with subjected to high risk both on the nest and reliably return. The lack of a protected site monogamous mothers. during foraging, failed before the first brood a subsocial open to higher per- At least in ants and other social Hyme- emerged (53). When foundresses of the Neo- capita mortality and lower per-capita avail- noptera, the reason for the monogamy win- tropical stenogastrine wasps Liostenogaster able food. (Compare, for example, the habitat dow principle is open to several alternative fralineata and Eustenogaster fraterna disappear, of a population of subsocial insects confined explanations that are relevant to the origin of the orphaned subordinate helpers, whether kin to the canopy of a single tree, exposed to the eusociality. The first explanation is based on or nonkin, rear her brood while starting their elements and enemies, with that of pop- direct observation of natural history. A single own. Thus, they create an “insurance-based” ulation of wasps living in a manufactured mating, with the sperm stored in the moth- advantage to the cooperators—and to the ’ fortress within a tree branch from which er s spermatheca, provides the same amount origin of eusociality (54, 55). scouts can travel abroad for food.) of genetic variation as matings by individual In summary, the monogamy window Once dispersal is silenced, the adult stay- solitary (noneusocial) species. Because the principle can be explained logically through at-home daughters immediately subordinate earliest eusocial colonies consist of a relatively direct observation as the consequence of themselves to their mother in the role of small number of individuals, the number individual-level natural selection. It exists nonreproductive workers. Why does this of sperm from a single mating (paid out because there is little relative advantage to seemingly non-Darwinian behavior occur, through the spermathecal valve) is adequate a foundress to mate more than once. The ’ even if only partially? The answer, for to last for the founding female susuallybrief advantage of acquiring greater genetic di- hymenopterans at least, is that adults have lifetime as queen. Another selection pressure versity in the small cohort of first offspring is a preexisting propensity to form dominance favoring this explanation of monogamy was outweighed by the protection afforded by hierarchies in which later occupants yield seldom invoked by previous authors but also a constructed nest. To the extent that some of rank to earlier occupants. Adults are strongly is confirmed by direct observation: The the early worker broods are fertile, as often predisposed (“spring-loaded”) to become mortality of the eusocial foundresses is very happens in primitively eusocial species, nat- eusocial when forcefully kept together. For high from the moment they leave the mother ural selection becomes multilevel: The fitness example, Ceratina and Lasioglossum bees, nest and mate until they finish constructing of the genomes of both the queen and each of when experimentally confined together in a nest. Time is of the essence in the interval her potentially reproductive workers derives very close quarters, proceed to divide labor between leaving the relative safety of the from their inherited traits expressed in early variously in foraging, tunneling, and guard- mother nest and entering the relative safety colonial life. ing of the nests (43–45). The dominant fe- of the new one. The agents of the increased Another consequence of the monogamy male stays at the nest as the reproductive mortality during exposure are many, both principleisthatthefirstoffspringofmo- caste. This propensity for forming domi- biological (chiefly through predation) and nogamous founding queens are closely nance hierarchies sets the stage for the evo- physical (because of the scarcity of nest sites related, as sisters. Primitively eusocial hyme- lution of eusociality. In one well-studied case, and hour-by-hour vicissitudes in the envi- noptera species are monogamous, as pointed with a pattern that may be widespread in ronment). The large magnitude of the out by Hughes et al. (56). Data are still temperate halictine bees, females mate in the resulting hecatomb of would-be foundresses lacking, but closely related solitary species are autumn and form multiple-female colonies has been commonly observed in species that under the same predation-selection pressure, in the spring. In each colony one of the release large numbers in nuptial flights. and they, too, can be expected to be mo- foundresses, as a rule the largest or oldest, Tschinkel (6), for example, has described the nogamous. Because there are hundreds of becomes the queen, guarding the nest en- death of the vast majority of imported fire extant related solitary species and only six trance and thereby inducing her cofoun- ant (Solenopsis invicta) queens from the first known hymenopteran eusocial lines, the dresses to function as workers (46, 47). minute they take flight, subjecting themselves kinship-based hypothesis of Hughes et al. “ Spring-loading as a step in the origin of to predation by and insects and the (56) does not explain why only a few of the eusociality did not come out of the blue. It is chance of heat death, starvation, execution, monogamous lines evolved eusociality. consistent with the fixed-threshold model and usurpation.” As the queens settle to the documented in the origin of division of labor ground, “a further fraction is taken by The Cretaceous Adaptive Radiation in well-formed insect societies. Behavioral ground-based predators, especially other Ants were born among dinosaurs of the studies have shown that, in general, members ants” (6). When predators are abundant, as Cretaceous Period (29–31). Most of their

Wilson and Nowak PNAS | September 2, 2014 | vol. 111 | no. 35 | 12587 Downloaded by guest on September 28, 2021 are found in cupressaceous amber which covered a much smaller fraction of in each of these species are fattened by the from New Jersey, Alberta, Siberia, and the land and which were farther poleward workers, and they grow massive wing mus- Myanmar (formerly Burma) and also as than is the case today. The soil and ground cles. In many species virgin queens and males fossils in rock compressions occurring in litter of angiosperm-dominated forests are, fly from the nest to form mating swarms. sub-Saharan Africa, Eurasia, and South and evidently always have been, far more Males mate once, and the queen, depending America. The still very imperfect emerging diversified in structure and physiochemical on species, mates once or several times. picture is a possible (but far from proven) conditions than those of more gymno- After mating each male dies, usually on the Gondwanan fauna featuring the myrmecio- sperm-dominated forests. In particular they day of mating and principally by predation. morph , represented today by Myrmecia inevitably created, as they do today, a much The newly inseminated queen, carrying the and Nothomyrmecia in Australia and the greater variety of both dwelling places and sperm within her spermatheca, flies a distance nearly worldwide Pseudomyrmecinae, and food for ants and other invertebrates. In that varies among species and then sets out to a Laurasian fauna, consisting of the extinct addition, both the diversity and abundance construct a nest and lay her first batch of eggs. sphecomyrmines and other contemporary of ants appear to have been greatly en- Thereafter she does not leave the nest to se- genera within or close to the poneroid clade. hanced by claustrality, an innovation in the cure food but instead feeds the growing larvae Of the derivative formicoid clade, destined colony life cycle that deserves special at- with regurgitated glandular food manufac- during the early Eocene to expand to vast tention in sociobiological theory. tured by materials and energy from her fat diversity and abundance worldwide, only bodies and catabolized wing muscles. By the asingleformicine,Kyromyrma neffi (57), The Claustral Revolution, Ecological time the first brood matures, typically emerg- and a dolichoderine, Chronomyrmex medi- Success, and Sex Allocation ing into adulthood as tiny, short-lived “minim cinehatensis (58), are known at present. Today, of the 21 extant ant subfamilies rec- workers,” her reserves are depleted. Tschinkel Also present were members of the Aneur- ognized by systematists as of 2013, four are (6) has appropriately characterized the queen etinae (represented today by a single, en- dominant in terms of geographic spread, ofthefireantSolenopsis invicta at this critical dangered species in Sri Lanka) and a population density, and species diversity: point as an “emaciated wraith.” She has raised species identified as either a primitive Ponerinae (1,264 known species, 8.59% of the a first brood of between 5 and 35 minims, who myrmeciine or a myrmeciine-sphecomyrmine total 14,710 known and described ant spe- thensetabouttoenlargethenestandsearch intermediate (59). cies), Dolichoderinae (828 known species, for food to feed her. On average the fire ant The limited diversity of documented Me- 5.63%), Myrmicinae (7,087 known species, queen’sweightduringherseclusion falls from sozoic species, despite the considerable 48.18%), and (3,794 known spe- 14 mg to about 7 or 8 mg. Because most of her breadth of their apparent adaptive radia- cies, 25.79%) (61). The ponerines, repre- stored reserves consisted of fat, which pos- tion, must result in part from the small sented by common species of Ponera and sesses higher per-gram caloric content than sample size of specimens available. However, Hypoponera, are especially abundant in the lean body components, the claustral fire ant in contrast to their overwhelming abundance litter and soil of tropical forests. Most of queen has lost two thirds of her starting total among insects in Eocene and later amber, their species form small colonies that feed energy reserve, much of it in maintenance cost. ants are genuinely scarce in Cretaceous am- primarily or exclusively on fresh prey or on The claustrality of queens in the For- ber (60). These lower densities may be a the remains of invertebrates newly killed by micinae, Myrmicinae, and Dolichoderinae consequence of the often small, cryptic col- other predators. However, they are out- confers an enormous advantage that is ob- onies and low population densities that numbered more than fivefold in species served routinely in field studies. The young characterize most phylogenetically primi- and individuals by the myrmicines (62). queen starts by acquiring a lifetime of sperm, tive species in the modern ant fauna. Above the ground, from several meters enough to last over a period of years to The most anatomically primitive ants from high to the canopy, the formicines and decades. She can fly a substantial distance the Mesozoic fauna were members of the dolichoderines dominate. from the mother nest—up to 8 km in Sol- extinct tribe Sphecomyrminae, the workers of In north temperate forests ants nest pri- enopsis invicta (63)—and then raise a force of which possessed a mosaic of ant and wasp marily on and in the ground and vegetational workers without leaving the safety of the nest traits—hence the name given them, “wasp litter. The species among them are over- in search of food. Claustrality thus removes ants.” The basal rooting of present-day whelmingly myrmicines and formicines. most of the threat from predators and also Martialinae and Leptanillinae places the ori- Monogynous (single-queened) colonies of from enemy ants of the same species (2, 6). gin and early diversification of ants as far species in the Myrmicinae, Formicinae, and Studies of both monogamous and polygy- back as Early Cretaceous times. Molecular Dolichoderinae, the world-dominant crown nous claustral ant species have revealed that phylogenetic studies of these and other living groups of the formicoid clade, share claus- the ratios of the number of queens to number species place the origin of almost all the living trality, the habit of the newly inseminated of males produced are close to but below the subfamilies in the early or middle Late Cre- queen of sealing herself in a chamber while 1:1 Fisherian ratio. On the other hand, the taceous or the Early Paleogene Periods (29– rearing her young. Claustrality is an evolu- ratio of energy costs invested in females vs. 31). The history of the ants as a whole, tionarily derived and nearly unique feature of malesisunderstandablymuchhigher.For however, appears not to extend as far back their life cycles. This trait is the decisive factor example, in one large dataset of 42 monogy- as the Jurassic Period (29–31). in the sex allocation of resources. It is de- nous (single mother queen) species summa- Evidently the key event fostering the phy- monstratively adaptive, appearing in fact to rized by Pamilo (64), the ratio of the number logenetic expansion of ants in general was the be basic to the ecological success of the three of virgin queens to males averaged 0.436, replacement in the mid-Cretaceous of a large subfamilies. Except in species that are socially whereas the ratio of energy costs invested in part of the predominantly - parasitic or in which mated queens rejoin the virgin queens vs. males averaged 0.631. dominated forest by the angiosperms (flow- mother colony (both of which also are de- Full claustrality is limited almost entirely to ering plants). These insects flourished rived traits in evolution), the virgin queens the subfamilies Myrmicinae, Formicinae, and in tropical to warm-temperate forests, are much larger than the males. The queens Dolichoderinae, and herein lies a point of

12588 | www.pnas.org/cgi/doi/10.1073/pnas.1405550111 Wilson and Nowak Downloaded by guest on September 28, 2021 considerable importance to sociobiological been that workers are in control and skew those of the mother queen exclusively during PERSPECTIVE theory. These three phylads dominate the the sex allocation to the virgin queens be- colony foundation as the targets of natural North Temperate Zone in colony and worker cause of their closer genetic relationship. selection. abundance and become increasingly domi- However, this assumption also is an error. nant poleward. American and European The mother queen, not the workers, is in Inadequacy of Inclusive Fitness and researchers have focused largely on North principal charge of which sex is preferred. Beyond Temperate species, and the result has been an If she “decides” to produce all females, she The evolution of social insects often is pre- unintended bias. For example, all but four of can hold her spermathecal valve open; if, sented as a testing ground for inclusive fitness the 40 species cited in Pamilo’s (64) study of on the other hand, her preference is all theory. It has been claimed that inclusive sex allocation belong to these three families, males, she can keep the valve closed. If she fitness can explain sex allocation, worker out of the 21 subfamilies worldwide. chooses a certain percentage of virgin policing, conflict resolution, and evolution of Full claustrality was derived from the basal queens and males, and the workers wish eusociality (14), but precise calculations of condition of partial claustrality, which is otherwise, the workers can change the ratio inclusive fitness do not exist for any of these practiced generally by the other subfamilies. by killing one sex or another, a process phenomena. Relatedness-based arguments, Thesameconditionoccursinsolitaryand observed in exsecta and Line- such as the monogamy window hypothesis, primitively eusocial bees and wasps that pithema humile (67, 68). However, the are not necessarily wrong but rarely provide progressively rear their young. In partial process is energetically costly, and there is a complete picture; moreover, one cannot claustrality the foundress, sometimes assisted no reason to assume that the advantage of rely on inclusive fitness to determine when temporarilybycooperatingfoundresses,rai- the culling is to the advantage of the they are correct. The failure of inclusive fit- ses the young in a nest but forages outside to workers as opposed to that of the queen ness theory to provide exact calculations is obtain part of the food supply (65). One rare and colony as a whole. Furthermore, there exception is the ponerine Pachycondyla lutea is no evidence at present that such culling is not surprising, because a mathematically (66), which is fully claustral. practiced widely, although very few studies meaningful approach to inclusive fitness (72) From the broad stock of partially claustral have addressed this issue. The workers also cannot be performed for the majority of clades have arisen several specialized life may inform the queen of the sex ratio evolutionary processes (5), and the linear cycles, including single-queen army ant col- needed, but such a feedback loop has yet to regression method (73–75) does not provide onies that multiply by fission. From the fully be found. meaningful insights and cannot make em- claustral subfamilies have emerged species Workers of the ant colony nevertheless pirical predictions (76). In general it is not and strains with polygynous colonies (mul- might be thought to control the production possible to study social evolution from the tiple queens) that multiply by budding (3, 4). of virgin queens (providing the queen choo- perspective of an individual by evoking the In this latter assemblage, young queens mate ses to create females in the first place) by virtual quantity of inclusive fitness. Instead on or near their home nests and return to the influencing the female larvae to develop into we should focus on how natural selection acts home nest to participate in reproduction. either virgin queens or workers. However, in on alleles that modify social behavior. On the Having no need to carry on-board reserves, the myrmicine Myrmica ruginodis,themost level of genes or alleles, there is no inclusive the virgin queens of polygynous species are thoroughly analyzed case of female caste fitness: Mathematical descriptions of the smaller in size and receive a resource in- determination in ants to date, at least five evolutionary dynamics of genetic mutations vestment from their mother colony more factors have been implicated. Emanating (in do not require a partition of fitness effects closely matching that provided to males. macrogyne colonies) variously from the (which usually is impossible anyway) or any Pamilo’s (64) estimate of the queen-to-male mother queen and the workers, these factors other aspect of inclusive fitness theory. We resource-investment ratios from 25 polygy- are larval nutrition, exposure to winter hi- advocate the development of precise theories nous species averaged 0.444, much closer to bernation nest temperature, queen presence that are grounded in a good understanding monogynous parity. Parasitic species in the or absence, egg size, and queen age (69, 70). same subfamilies also need no on-board re- The condition of the egg before leaving the of the life cycles and evolutionary history serves. As also expected, in slave-making spe- oviduct also has been implicated in the for- of social insects.

cies the queen-to-male resource-investment micine Formica polyctena (71). The relative ACKNOWLEDGMENTS. Without implying responsibility ratios have been found to be close to parity importance of these factors and the degree of for factual errors that may remain or particular interpre- (average 0.483). their interactions have not been worked out, tations we have drawn, we thank the following for very helpful reviews of the present article: S. Bowles, S. Brady, Taking the evolutionary history of the ants but collectively they point either to the phe- H. Gintis, S. Kocher, D. J. C. Kronauer, D. Lubertazzi, into account, and from direct inspection of notypic traits of the colony as a whole or to C. Rabeling, C. E. Tarnita, B. L. Thorne, and P. S. Ward. colony founding in modern species, it is quite clear that the pattern of sex allocations can be

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