Gowdy & Krall (G&K) propose that the origins of ant eusociality and human ultrasociality are fundamentally economic, necessitated by the demands of agriculture, which led to striking divisions of labor. Among these tasks are those based on sex and reproduction, which are dramatically different in insects and humans. The authors' focus on managed agriculture obscures the role that divisions of sex and reproductive labor may have played in the development of eusociality and collective economic activity, including relative to hunting and gathering.
Because food cultivation has emerged in only four types of animals – ants, termites, humans, and ambrosia beetles – similar evolutionary mechanisms are suspected to have driven its development (Schultz & Brady Reference Schultz and Brady2008). However, proving the hypothesis and identifying the common mechanisms “requires an understanding of the historical sequence of events that generated each system” (Schultz & Brady Reference Schultz and Brady2008, p. 5438), which is hard to come by. Large-scale phylogenetic analyses of termite species have failed to identify even the origin of “true workers” (Inward et al. Reference Inward, Vogler and Eggleton2007).
Researchers studying these four types of animals, and the only eusocial mammal, independently conclude that the shift from the care of young by parents to care by others (alloparenting) played a critical role in the development of eusociality – if not in food cultivation, which in some orders (notably, beetles) can occur in the absence of eusociality (Biedermann & Taborsky Reference Biedermann and Taborsky2011).
In terms of phylogeny, reproduction and development, and agricultural subsistence, ants and termites highlight how variation in critical parameters can make it very difficult to determine the ecological constraints or evolutionary mechanisms involved.
Termites developed from a “social cockroach” about 130 million years ago, and evolved eusociality just once. They are diploid with a somewhat equal, albeit complex sex ratio, and with altricial offspring that are frail, dependent, and lack the intestinal symbionts necessary for the complex metabolic processes that sustain both organisms (Nalepa Reference Nalepa2015). Cladistics and life history analysis suggest that the shift to alloparental care of altricial offspring was the “tipping point” in the evolution of termite eusociality (Nalepa Reference Nalepa2015). Phylogenetic analyses of 250 termite species suggest that fungus-growing evolved from wood-feeding and may have been the ancestral condition, with soil-feeding lineages developing from the ancient fungus growers, and wood-feeding re-evolving (Inward et al. Reference Inward, Vogler and Eggleton2007). Insect agriculture thus is not evolutionarily recent.
Hymenoptera evolved eusociality independently in 11 different lineages (Korb Reference Korb2007), and fungus-growing once (Mueller et al. Reference Mueller, Gerardo, Aanen, Six and Schultz2005). Cutting leaves to feed fungi is a recent development (about 8–10 million years ago), as is the complex social organization featuring striking morphological differences among different workers that evolved with it (Schultz & Brady Reference Schultz and Brady2008). Eusocial hymenoptera are haplodiploid: Unfertilized eggs become male. Workers in all castes are overwhelmingly female; males serve principally reproductive roles (Wilson & Hölldobler Reference Wilson and Hölldobler2005). The single-stage larvae are helpless, requiring extensive care.
The fungus-growing haplodiploid ambrosia beetle Xyleborinus saxesensii is primitively eusocial (Biedermann & Taborsky Reference Biedermann and Taborsky2011). Although each female is capable of breeding and establishing her own “gallery,” group members engage in the diverse cooperative tasks involved in brood care, gallery maintenance (fungiculture, digging, defense, waste disposal), and grooming of adults and larvae. Although free to mate themselves, females tend to remain in the natal gallery if brood size is large, requiring greater care, but will disperse when numbers of mature females relative to brood is high (Biedermann & Taborsky Reference Biedermann and Taborsky2011). Alloparenting thus appears to be privileged over personal reproduction.
Cooperative brood care is also thought to ground the evolution of eusociality in two genera of African mole rat, which dwell in subterranean colonies, harvest tubers, and are thought to be the only mammals to have evolved eusociality (Burda et al. Reference Burda, Honeycutt, Begall, Locker-Grütjen and Scharff2000). Reproduction in eusocial mole rats is limited to queens that mate with one to three males, while workers engage in brood care, food gathering, digging, cleaning, and collective defense. Alloparenting is critical because mole-rat queens don't store fat and require regular provisioning during gestation and lactation, which are longer in these genera. Reproductive strategies diverge greatly. In naked mole-rat colonies, reproductive capacity in both sexes is equally suppressed, and more than 99% of offspring never reproduce (Faulkes & Bennett Reference Faulkes and Bennett2001). Colonies are highly inbred, and are reported to have a higher degree of relatedness (0.8%) than hymenoptera colonies (Faulkes & Bennett Reference Faulkes and Bennett2001). By contrast, Damaraland mole rats cannot breed with nest-mates, and only female reproductive capacity is dramatically suppressed. Nevertheless, up to 90% of colony members never breed (Faulkes & Bennett Reference Faulkes and Bennett2001).
The human case is more complex due largely to culture, as G&K note. However, allomaternal care is increasingly recognized as a critical precursor to the evolution of complex human social organization and advanced labor specialization (Smaldino et al. Reference Smaldino, Newson, Schank and Richerson2013). Allomaternal care is the best predictor of prosociality among primates (Burkart et al. Reference Burkart, Allon, Amici, Fichtel, Finkenwirth, Heschl, Huber, Isler, Kosonen, Martins, Meulman, Richiger, Rueth, Spillmann, Wiesendanger and Van Schaik2014), and helps to explain significant differences in the life histories of human females compared to other apes, such as long childhoods, menopause, and long post-reproductive life (Mace Reference Mace2013).
Among contemporary hunter-gatherers, alloparenting is commonplace, as is food sharing and cooperative foraging with unrelated individuals (Dyble et al. Reference Dyble, Salali, Chaudhary, Page, Smith, Thompson, Vinicius, Mace and Migliano2015). These groups are widely known to be egalitarian and to pair-bond. Gender equality probably coevolved with higher offspring costs, the need for biparental investment, and the advantages of circulating through networks of kin (Dyble et al. Reference Dyble, Salali, Chaudhary, Page, Smith, Thompson, Vinicius, Mace and Migliano2015). Paradoxically, although foragers of both sexes prefer living with close relatives, they invariably live with high proportions of unrelated individuals. Recent modeling experiments and field observations suggest that shared influence in decisions about group composition is the most probable cause (Dyble et al. Reference Dyble, Salali, Chaudhary, Page, Smith, Thompson, Vinicius, Mace and Migliano2015). Greater influence by one sex results in higher relatedness within the group, and a bias in fitness benefits advantageous to the sex with the most influence (usually male).
The consistency of the association between eusociality and alloparenting of altricial young, with a somewhat lesser correspondence with female-biased sex ratios, suggests that significant fitness benefits accrue to a division of labor in breeding and alloparenting. These reproductive economics provide a platform for enhanced subsistence strategies, with symbiotic food cultivation and agriculture being two possibilities.
Understanding the differences in reproductive organization and their implications for structuring sociality more generally is essential for determining whether the same evolutionary forces are at work in the evolution of eusociality in agricultural insects and ultrasociality in agricultural humans – as G&K suggest – or whether a resemblance of outcomes has arisen from different forces.
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Gowdy & Krall (G&K) propose that the origins of ant eusociality and human ultrasociality are fundamentally economic, necessitated by the demands of agriculture, which led to striking divisions of labor. Among these tasks are those based on sex and reproduction, which are dramatically different in insects and humans. The authors' focus on managed agriculture obscures the role that divisions of sex and reproductive labor may have played in the development of eusociality and collective economic activity, including relative to hunting and gathering.
Because food cultivation has emerged in only four types of animals – ants, termites, humans, and ambrosia beetles – similar evolutionary mechanisms are suspected to have driven its development (Schultz & Brady Reference Schultz and Brady2008). However, proving the hypothesis and identifying the common mechanisms “requires an understanding of the historical sequence of events that generated each system” (Schultz & Brady Reference Schultz and Brady2008, p. 5438), which is hard to come by. Large-scale phylogenetic analyses of termite species have failed to identify even the origin of “true workers” (Inward et al. Reference Inward, Vogler and Eggleton2007).
Researchers studying these four types of animals, and the only eusocial mammal, independently conclude that the shift from the care of young by parents to care by others (alloparenting) played a critical role in the development of eusociality – if not in food cultivation, which in some orders (notably, beetles) can occur in the absence of eusociality (Biedermann & Taborsky Reference Biedermann and Taborsky2011).
In terms of phylogeny, reproduction and development, and agricultural subsistence, ants and termites highlight how variation in critical parameters can make it very difficult to determine the ecological constraints or evolutionary mechanisms involved.
Termites developed from a “social cockroach” about 130 million years ago, and evolved eusociality just once. They are diploid with a somewhat equal, albeit complex sex ratio, and with altricial offspring that are frail, dependent, and lack the intestinal symbionts necessary for the complex metabolic processes that sustain both organisms (Nalepa Reference Nalepa2015). Cladistics and life history analysis suggest that the shift to alloparental care of altricial offspring was the “tipping point” in the evolution of termite eusociality (Nalepa Reference Nalepa2015). Phylogenetic analyses of 250 termite species suggest that fungus-growing evolved from wood-feeding and may have been the ancestral condition, with soil-feeding lineages developing from the ancient fungus growers, and wood-feeding re-evolving (Inward et al. Reference Inward, Vogler and Eggleton2007). Insect agriculture thus is not evolutionarily recent.
Hymenoptera evolved eusociality independently in 11 different lineages (Korb Reference Korb2007), and fungus-growing once (Mueller et al. Reference Mueller, Gerardo, Aanen, Six and Schultz2005). Cutting leaves to feed fungi is a recent development (about 8–10 million years ago), as is the complex social organization featuring striking morphological differences among different workers that evolved with it (Schultz & Brady Reference Schultz and Brady2008). Eusocial hymenoptera are haplodiploid: Unfertilized eggs become male. Workers in all castes are overwhelmingly female; males serve principally reproductive roles (Wilson & Hölldobler Reference Wilson and Hölldobler2005). The single-stage larvae are helpless, requiring extensive care.
The fungus-growing haplodiploid ambrosia beetle Xyleborinus saxesensii is primitively eusocial (Biedermann & Taborsky Reference Biedermann and Taborsky2011). Although each female is capable of breeding and establishing her own “gallery,” group members engage in the diverse cooperative tasks involved in brood care, gallery maintenance (fungiculture, digging, defense, waste disposal), and grooming of adults and larvae. Although free to mate themselves, females tend to remain in the natal gallery if brood size is large, requiring greater care, but will disperse when numbers of mature females relative to brood is high (Biedermann & Taborsky Reference Biedermann and Taborsky2011). Alloparenting thus appears to be privileged over personal reproduction.
Cooperative brood care is also thought to ground the evolution of eusociality in two genera of African mole rat, which dwell in subterranean colonies, harvest tubers, and are thought to be the only mammals to have evolved eusociality (Burda et al. Reference Burda, Honeycutt, Begall, Locker-Grütjen and Scharff2000). Reproduction in eusocial mole rats is limited to queens that mate with one to three males, while workers engage in brood care, food gathering, digging, cleaning, and collective defense. Alloparenting is critical because mole-rat queens don't store fat and require regular provisioning during gestation and lactation, which are longer in these genera. Reproductive strategies diverge greatly. In naked mole-rat colonies, reproductive capacity in both sexes is equally suppressed, and more than 99% of offspring never reproduce (Faulkes & Bennett Reference Faulkes and Bennett2001). Colonies are highly inbred, and are reported to have a higher degree of relatedness (0.8%) than hymenoptera colonies (Faulkes & Bennett Reference Faulkes and Bennett2001). By contrast, Damaraland mole rats cannot breed with nest-mates, and only female reproductive capacity is dramatically suppressed. Nevertheless, up to 90% of colony members never breed (Faulkes & Bennett Reference Faulkes and Bennett2001).
The human case is more complex due largely to culture, as G&K note. However, allomaternal care is increasingly recognized as a critical precursor to the evolution of complex human social organization and advanced labor specialization (Smaldino et al. Reference Smaldino, Newson, Schank and Richerson2013). Allomaternal care is the best predictor of prosociality among primates (Burkart et al. Reference Burkart, Allon, Amici, Fichtel, Finkenwirth, Heschl, Huber, Isler, Kosonen, Martins, Meulman, Richiger, Rueth, Spillmann, Wiesendanger and Van Schaik2014), and helps to explain significant differences in the life histories of human females compared to other apes, such as long childhoods, menopause, and long post-reproductive life (Mace Reference Mace2013).
Among contemporary hunter-gatherers, alloparenting is commonplace, as is food sharing and cooperative foraging with unrelated individuals (Dyble et al. Reference Dyble, Salali, Chaudhary, Page, Smith, Thompson, Vinicius, Mace and Migliano2015). These groups are widely known to be egalitarian and to pair-bond. Gender equality probably coevolved with higher offspring costs, the need for biparental investment, and the advantages of circulating through networks of kin (Dyble et al. Reference Dyble, Salali, Chaudhary, Page, Smith, Thompson, Vinicius, Mace and Migliano2015). Paradoxically, although foragers of both sexes prefer living with close relatives, they invariably live with high proportions of unrelated individuals. Recent modeling experiments and field observations suggest that shared influence in decisions about group composition is the most probable cause (Dyble et al. Reference Dyble, Salali, Chaudhary, Page, Smith, Thompson, Vinicius, Mace and Migliano2015). Greater influence by one sex results in higher relatedness within the group, and a bias in fitness benefits advantageous to the sex with the most influence (usually male).
The consistency of the association between eusociality and alloparenting of altricial young, with a somewhat lesser correspondence with female-biased sex ratios, suggests that significant fitness benefits accrue to a division of labor in breeding and alloparenting. These reproductive economics provide a platform for enhanced subsistence strategies, with symbiotic food cultivation and agriculture being two possibilities.
Understanding the differences in reproductive organization and their implications for structuring sociality more generally is essential for determining whether the same evolutionary forces are at work in the evolution of eusociality in agricultural insects and ultrasociality in agricultural humans – as G&K suggest – or whether a resemblance of outcomes has arisen from different forces.