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Kin-selected cooperation without lifetime monogamy: human insights and animal implications
Opinion
Kin-selected cooperation without lifetime monogamy: human insights and animal implications Karen L. Kramer1,2 and Andrew F. Russell2,3 1
Department of Anthropology, University of Utah, Salt Lake City, UT 84112, USA Department of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA 3 Centre for Ecology and Conservation, College of Life and Environmental Sciences, University of Exeter, Penryn TR10 9FE, UK 2
Recent phylogenetic analyses suggest that monogamy precedes the evolution of cooperative breeding involving non-breeding helpers. The rationale: only through monogamy can helper–recipient relatedness coefficients match those of parent–offspring. Given that humans are cooperative breeders, these studies imply a monogamy bottleneck during hominin evolution. However, evidence from multiple sources is not compelling. In reconciliation, we propose that selection against cooperative breeding under alternative mating patterns will be mitigated by: (i) kin discrimination, (ii) reduced birth-intervals, and (iii) constraints on independent breeding, particularly for premature and post-fertile individuals. We suggest that such alternatives require consideration to derive a complete picture of the selection pressures acting on the evolution of cooperative breeding in humans and other animals. Ancestral mating and contemporary cooperation Humans routinely rely on others to help rear their young, and therefore should be characterized as cooperative breeders [1–5]. Given that cooperative breeding is not shared with other great apes, it was likely derived during hominin evolution. The question is: what facilitated this evolutionary transition in hominin? One hypothesis is that lifetime monogamy favors cooperative breeding because long-term mate-fidelity raises the relatedness among successive siblings to be equivalent to that between parents and offspring [6] (Box 1). Recently, phylogenetic studies have provided compelling evidence that the evolution of monogamous mating patterns preceded the evolution of cooperative breeding across a variety of insect, bird, and mammal species [7–9]. These studies hint that monogamy provides a general rule for explaining evolutionary transitions to cooperative societies (monogamy hypothesis [10]). As such, could the prevalence of cooperative breeding observed in contemporary human societies reflect a monogamous past in hominins? Corresponding author: Russell, A.F. ([email protected]). Keywords: alloparenting; kin discrimination; interbirth intervals; juvenile helpers and grandmothers; mating system; monogamy hypothesis. 0169-5347/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2014.09.001
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We readdress here the question of whether monogamy was prevalent during hominin evolution and, given that the evidence is weak, provide alternative means by which kin-based cooperation could be selected other than through lifetime monogamy. Specifically, we (i) describe cooperative breeding systems in animals, and outline the recent evidence providing general support for the monogamy hypothesis; (ii) highlight that human cooperative breeding systems are not exceptional; (iii) assess the evidence for the monogamy hypothesis in humans using a broad literaturebase; and (iv) provide several alternatives to the monogamy hypothesis for explaining the evolution of kin-based cooperative breeding. We do not attempt an exhaustive review of selection on cooperative breeding; our specific intention is to address whether monogamy was a necessary precondition for cooperative breeding in humans. We find little compelling evidence, and propose that lifetime monogamy is not required to select for cooperative breeding when kin discrimination is likely, birth-intervals are short, and individuals are not currently able to breed independently. Apparent commonalities in cooperative breeders Cooperative breeding describes a system in which individuals help in the reproductive attempts of others. This situation presents a classic evolutionary puzzle because helping should incur a cost to one’s own current or future direct reproductive success. Despite this, cooperative breeding has evolved numerous times within and across diverse taxa including insects, spiders, crustaceans, fish, birds, and mammals [2,10]. Across nonhuman cooperative breeders, individuals who provide care to the offspring of others are usually, but not always, nonbreeders [2,7– 12]. In the hymenoptera (bees, wasps, ants), helpers (or workers) tend to be fertile or sterile adults [8], while in the isoptera (termites) they are often totipotent juveniles [10]. In birds, helpers tend to be sexually mature [2,7], while in mammals premature helpers are common [2,11–14] and post-fertile helpers occur in two whale species [15]. Although variability exists across cooperative breeders in the modes of help provided, status of helpers, group size and mating systems [2,7–12], recent phylogenetically based comparative analyses reveal an apparent commonality
Opinion Box 1. The role of monogamy in selecting for cooperative breeding The strengths of the monogamy hypothesis lie with its simplicity and sound foundation in inclusive fitness theory [6,10]. The inclusive fitness of individuals is governed by their direct + indirect (through collateral kin) genetic contributions to following generations. Consider the general case that each parent can propagate 50% of their genes for any offspring produced. Under monogamy, each offspring produced in a group also shares 50% of its genome, on average, with subsequent offspring in the same group. Thus, where parents are faithful within and between attempts, recruits to the group will be as related to subsequent offspring as they would be to their own. Consequently, at sexual maturity the fitness accruable to previous offspring from helping to rear subsequent offspring coaligns with that of rearing one’s own [relatedness (r) = 0.5 in each case]. This is not automatic under any other mating system (see Table 1 in main text, but see Box 2 for an exception under polygyny). Under all others, female offspring will be more related on average to their own offspring (r = 0.5) than to others produced subsequently in their group (r = 0.25–0.5; less if mothers produce offspring jointly or communally). For male offspring, the story is more complicated because, assuming they know their mother, males can be more related to subsequent offspring produced in the group (r = 0.25–0.5) than they are to their ‘own’ under both polyandrous and promiscuous mating systems (r = 0–0.5). The paradoxical role of high female infidelity on tendencies for sons to cooperate instead of attempt independent breeding has not been addressed. This latter caveat aside, it is easy to see how parental fidelity can have an influential, perhaps defining, role in selecting individuals to stay and help rather than disperse and breed.
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probabilities and extents of help provided by close relatives [20,21]. Given the illuminating results from phylogenetic analyses highlighting the evolutionary relationship between monogamy and cooperative breeding (see above), it is tempting to hypothesize that the prevalence of cooperative breeding in our own species implies a monogamous past.
[10]. First, Hughes et al. [8] conducted a phylogenetic analysis of 267 species of hymenoptera from eight lineages with independent evolutionary origins. Despite variation in modern mating systems (monandry, polyandry, polygyny; see Table 1), they found that monandry was generally the ancestral state to the evolution of cooperative breeding. Second, the importance of monogamy for the evolution of cooperative breeding was replicated in birds. Phylogenetic analysis of 267 bird species showed that cooperative species were threefold less promiscuous on average than noncooperative species [7], and species of non-cooperative ancestors were twice as likely to evolve cooperative breeding if they tended towards monogamy. In a third study, cooperative breeding among mammals was shown to be concentrated in species where females mate exclusively with a single male [9]. In a phylogenetic reconstruction of 1874 mammal species, evolutionary transitions to cooperative breeding were likely associated with monogamy.
Evidence for monogamy in humans? Behavioral evidence: contemporary mating patterns Mating patterns as observed in contemporary small-scale societies, especially hunter-gatherers, which do not have the confounding influences of modern medicine and contraception, are frequently used to make inferences about the past. Across these societies, humans live in multimale– multifemale groups which include multiple breeding females within socially recognized long-term bonds. While such bonds exist in all human societies, these need not be monogamous, and frequently include polygynous and occasionally polyandrous configurations, which vary both within and across societies [22–27]. Although polygynous marriage is sanctioned in 80–85% of traditional human societies [24], this figure is based on cultural norms, not on individual behaviors. Closer scrutiny of these data reveals that cross-sectionally the majority of individuals within a society are currently married monogamously. Notwithstanding, longitudinal data show that men also accumulate wives during their lifetimes and, even where bonds are monogamous, they tend to be serially so in both sexes owing to high mortality and divorce rates, as well as asymmetries in the termination of fertility [25,28]. Paternity outside a pair-bond (promiscuity; but see Table 1 for definitions in cooperative vertebrates) is seldom studied but seems to be limited. A human extra-pair paternity rate of 9% is often quoted, but this study was based on a small number of samples and its design has been critiqued for several reasons [29]. The most thorough cross-cultural study suggests a median nonpaternity rate of 1.7–3.3% depending on sample [30], with the highest known extramarital paternity in a traditional society being about 9% (e.g., the Yanomamo, although estimates vary depending on sampling method) [31]. That humans commonly show paternal care, which also likely evolved following the split from other great apes, is further suggestive of limited promiscuity and strong inter-sexual mate bonds [32].
Cooperative breeding in humans The defining features and characteristics of cooperative breeding introduced above unquestionably apply to modern humans. Across traditional, preindustrial and marketintegrated societies, parents receive substantial, although cross-culturally variable, help particularly from pre-fertile juveniles of both sexes and post-fertile females [4,16]. Help from juveniles and post-fertile females has been shown to have significant consequences for maternal energy expenditure and fitness, primarily through reducing birth intervals and offspring mortality [17–19]. Although humans also are associated with more generalized patterns of cooperation, as in nonhuman cooperative breeders, case studies in traditional human societies reveal preferential
Synthesis Socially monogamous pair-bonds are prevalent in extant human societies, but partners frequently change and any monogamy is often serial (Table 1). In this regard, humans are like all vertebrates but contrast starkly with many cooperative insects which display lifetime fidelity [10]. From the perspective of breeders, the fitness consequences of serial monogamy might differ little from those of lifetime monogamy. However, for a helper the two systems are very different, with serial monogamy equating to polygyny or polyandry when the natal sex is replaced (system depends on which sex is philopatric), and promiscuity when the dispersing sex is replaced (Table 1). In addition, across human societies, a single male is not uncommonly 601
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Table 1. Glossary: mating systems, estimated prevalence in cooperative breeders and outcomes for relatedness among siblingsa Mating system Monandry
Definition Female mates with one male in her life before egg-laying
Example systems Many hymenopteran insects
Monogamy
One female pairs with one male (social) or mates with one male (genetic) One female mates with > 1 male (vertebrates: includes only withingroup males)
Termites, most birds, many mammals including humans
Polyandry
Polygyny
Hymenoptera: > 1 queen per colony; others: 1 male mating with >1 female within the group
Promiscuity
Female infidelity arising with males outside the pair-bond (humans) or outside the group (other animals) Identity of partner changes between reproductive events, through death, divorce, usurpation
Between-attempt infidelity (e.g., serial monogamy)
Common in advanced eusocial hymenoptera; relatively common in birds, fish, and mammals; exceptional in humans Common in hymenoptera, occurs birds and mammals, including humans
Common in birds, occurs in mammals and humans All vertebrates, including humans
General outcome All offspring born during the life of a queen have the same parents; the genes of the sire die with queen. Depends on infidelity: in termites infidelity is exceptional, in mammals it is low and in birds it is highly variable (see below). Depends on male–male relatedness (r): 0 in eusocial insects, generally high in mammals, and variable in birds. All else being equal, leads to among-sibling r values of 0.25–0.5. Polygyny dilutes group r values. Consequences depend on kin discrimination [easy if mothers clutch/birth at different time or place (plural breeding; among-sib r = 0.5); but not if same time or place (communal/joint-nesting, among-sib r = 0.25–0.5 – same father but different multiple mothers]. Depends on level of infidelity, but will push among-sibling r levels closer to 0.25 because fathers will tend to be unrelated. Potentially dramatic: even assuming withinattempt monogamy – replacement of the natal versus dispersing sex leads to r values between successive offspring of 0.25–0.375 and of 0.25, respectively.
a
Note that definitions are presented as applied to cooperative breeders, and may or may not be generalizable to other systems.
bonded with multiple females at some point in his life (simultaneous polygyny). Thus both serial monogamy and polygyny represent common mating patterns in humans; the relative importance of each during our evolutionary history is difficult to assess. Although mating patterns in contemporary societies are often used as analogies to the past, the diversity we see today might be evolutionarily derived following migration into new and contrasting ecologies [7–9]. Consequently we turn to anatomical signatures of ancestral mating patterns. Morphological evidence: sexual size dimorphism and testis size Anatomical traits, being less plastic than behavioral ones, take longer to modify following a change in selection pressure. As such, current morphology can be integrated with fossil evidence to elucidate evolutionary responses to ancestral selection pressures. Below we consider two morphological traits commonly used to make inferences about past mating patterns: sexual size dimorphism and primary sexual traits in the form of testis size. Sexual dimorphism Modern human body size dimorphism is relatively modest, slightly greater compared to other monogamous primates, but much less compared to polygynous species [33]. In fossil specimens, the general consensus has been that stature dimorphism was greater in the past and has diminished during hominin evolution, suggesting a decline in male–male competition. Some argue that size dimorphism in australopithecines was sufficiently attenuated to suggest an early monogamous and male provisioning ancestor [34]. Others are persuaded that the level of skeletal 602
dimorphism in australopithecines was sufficiently dimorphic [35] to suggest a male reproductive strategy focused on monopolizing females [36]. In light of these conflicting views, Plavcan [37] cautions that, although dimorphism indicates some degree of male agonistic competition, it is not a reliable indicator of mating behavior in extinct species. All that we can say for apparent certainty is that, if our last common ancestor were ‘gorilla-like’, we have become less dimorphic and less polygynous, and if it were ‘chimp-like’ we have maintained levels of dimorphism but have become less promiscuous. Either way, it is not clear from the sexual size dimorphism evidence that humans were ever fully monogamous. Testis size Sperm competition, associated with polyandrous or promiscuous matings, should be manifest in large testes relative to body size [38]. Humans have slightly smaller testes than predicted from body size, suggesting low female promiscuity [39]. Adjusting for body size, human testes are considerably smaller than those of chimpanzees, suggesting selection against female promiscuity, but somewhat larger than other monogamous primates [38]. A recent reanalysis, including a broader spectrum of populations, shows that humans encompass the range of variation for polygynous gorillas and orangutans, but not promiscuous chimpanzees, which is consistent with pair-forming polygynous or (serially) monogamous species [33]. While testis size is a predictor of female promiscuity, it is often mistakenly used as an indicator of monogamy. However, it cannot discriminate between monogamy and harem-based polygyny because in both cases sperm competition is expected to be relatively low [33,40].
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Box 2. Empirical shortcomings with the monogamy hypothesis and directions for future research There are three problems for the monogamy hypothesis when applied to vertebrates and some invertebrates. (i) The lack of compelling evidence for a monogamous past in hominin is not exceptional: phylogenetic analyses also suggest that monogamy did not precede cooperative breeding in a notable number of extant bird species [49]. (ii) While the phylogenetic analyses in birds also showed that an evolutionary history of promiscuity has selected against cooperative breeding in a significant number of cases, there are again important exceptions. For example, Australian fairy-wrens are one of the most promiscuous species so far documented, but most (if not all) remain cooperative breeders [50]. (iii) While individuals breed monogamously, no vertebrate species is lifetime monogamous; mortality, divorce, and usurpation are common. Thus, other factors clearly select for kin-selected cooperative breeding, and the question is what are they? Below we set out the more salient and testable additional (or alternative) hypotheses to the monogamy hypothesis for species lacking lifetime monogamy, while maintaining the theme of a general role of relatedness. Note that mating systems include serial scenarios (i.e., between-attempt infidelity; see Table 1 in main text). Hypothesis Kin discrimination allows cooperative breeding to evolve under alternative mating patterns Plural breeding increases scope for kin discrimination; hence cooperative breeding
Rationale/explanation First-order relatives can be helped under polygyny when mothers can be identified (see Table 1 in main text and below) Where eggs/offspring are delivered in different locations, bonds between mother and offspring will arise
Reduced birth-intervals increases relatedness among successive sibs
Vertebrates are prone to infidelity through partner loss; reduced birth intervals will mitigate this Low opportunity costs; relatedness to those they help exceeds 0 (0.25–0.5), regardless of mating system No individual is equal and many offspring fail to secure reproductive positions in life
Juvenile and post-fertile helping can be selected without monogamy Reduced outside reproductive options for fertile individuals will increase selection for helping lower orders of relatives High promiscuity selects for male helpers
Sons are often more related to mother’s offspring than to their ‘own’
Synthesis Several lines of morphological evidence appear to rule out strong promiscuity or polyandry in our recent past, but are unable to distinguish between monogamy and polygyny, or the extents and patterns of serial monogamy. The bestsupported conclusion seems to be that monogamy is firmly within, but not exclusive to, the repertoire of human mating strategies. Nevertheless, there is ambiguity about its time-depth, whether it relates to the evolution of cooperative breeding, and whether inter-sexual bonding developed in the context of a polygynous or monogamous breeding system. Because evidence can be found to characterize human breeding systems in a variety of ways, we caution against definitive views that rally partial evidence to forward particular perspectives. Cooperative breeding without (lifetime) monogamy The evidence for hominins passing through a monogamy bottleneck and emerging as a cooperative breeder is not particularly strong. This leads to two related questions. First, is the comparative evidence from other vertebrates sufficiently compelling to convince us that humans must have had a monogamous past, irrespective of the evidence? Second, are there alternative routes to kin-selected cooperative breeding other than through the evolution of monogamy? Below we focus on the latter and propose three main alternatives to the model that a monogamous past is a necessary prerequisite for the evolution of cooperative breeding through kin selection (Box 2). Our aim is not to undermine a facilitating role of monogamy in the evolution of cooperative breeding, but to illustrate that additional
Appropriate model systems Vertebrate species showing polygyny
Many species: plural breeding is more common than accredited, and is often confused with communal breeding where females deliver simultaneously in the same place All species: key unanswered question – how do ancestral birth intervals predispose species to cooperation? Mammals including humans; eusocial insects
All species: key unanswered question – how does probability of breeding at a given age or level of condition relate to selection for cooperation? Birds: promiscuity common
(or alternative) mechanisms can enable kin-selected cooperative breeding in the absence of lifetime monogamy (Box 2). Kin discrimination A benefit of lifetime monogamy in selecting for cooperative breeding is that all successive siblings are always related by an equivalent to one’s own offspring (Box 1). Kin discrimination reduces a requirement of (lifetime) monogamy in the evolution of cooperative breeding through kin selection because it allows offspring to help only when close-kin are available. Comparative analysis in cooperative birds shows that kin discrimination is an important mechanism ensuring kin-biased cooperation in groups where individuals vary in relatedness [41]. Whether or not kin discrimination can offer a suitable alternative selective force for cooperative breeding in the absence of lifetime monogamy depends on several other factors. For example, consider a group of animals where multiple females lay eggs or deliver live offspring simultaneously in the same nest or burrow (i.e., so-termed joint-nesting or communal breeding). The ability of offspring to recognize their mother will be near impossible in the egg-laying scenario and challenging in the viviparous one. By contrast, identifying mothers become significantly more efficient if multiple mothers in the same group breed plurally; in other words, in a different location or time, as is the case in humans. Under plural breeding, it is irrelevant whether or not each female has her own mate (monogamy) or shares a mate with other females (polygyny), because in both cases successive sibs have the same parents and will be as related to each other 603
Opinion as to their own offspring (assuming no parental death). While male tenure lengths are reduced in polygynous species compared with monogamous ones, in most cases males still survive successive births [42], allowing many offspring to direct care towards full siblings. Thus, all else being equal, monogamy need not elevate relatedness among successive sibs any more than polygyny provided that mothers can be reliably identified and fathers survive to sire successive births. Interbirth intervals In great apes, the likelihood that successive siblings will be related is partially reduced by the length of birth intervals. Because birth intervals are long (4–8 years), they often exceed the tenure of the dominant male and, regardless of breeding system, negatively affect the probability that successive offspring will be full siblings. Relative to the great apes, humans have considerably shorter birth intervals, which, in conjunction with the fact that helpers in humans are often subadults (see below), increases the probability that full-sibs can be helped under polygyny or serial monogamy. Whether or not species with short birth intervals are more likely to evolve cooperative breeding has not been tested. It is at least noteworthy that cooperative birds are most prevalent in Australia and Africa where selection to breed repeatedly within short and unpredictable rains is often intense. Although reduced birth intervals are generally thought of as being a consequence, rather than a cause, of cooperative breeding, the near ubiquity of this helper effect across cooperative societies is intriguing. One possibility is that reduced birth intervals are partly selected by parent(s) maximizing the probability that successive siblings are first-order relatives and hence that they receive maximal help with offspring care. We hypothesize that short birth intervals will facilitate the evolution of cooperative breeding and, following its evolution, be under selection to shorten further to capitalize on kin-biased helper investment strategies. Premature and post-fertile helpers The role of monogamy in the evolution of cooperative breeding might depend on the status of predominant helper types. For sexually fertile individuals, the fitness incentive to delay reproduction and help might be low where potential recipients have a relatedness (r) of less than 0.5 (Box 1 and Table 1), although this will be condition- or quality-dependent (see below). By contrast, for the premature (e.g., juvenile or sub-adult age classes) or post-fertile (e.g., grandmothers), no scope for accruing current direct fitness exists. For the former, helping provides an opportunity to gain immediate indirect fitness [43], which might have negligible detriment to future direct fitness, particularly given a significant time-frame to recoup any costs (see below). For the latter, helping represents the only way to gain any further fitness. As such, for each, we might expect that r levels below 0.5 between donor and recipient are sufficient to select for cooperative breeding. In birds, premature helpers are uncommon and seldom effective, while post-fertile helpers are not known. By contrast, in mammals, premature [11–14] helpers can represent a significant part of the workforce for many 604
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species, as do post-fertile helpers in some cases [15]. The key point we wish to make here is that for both juveniles and grandmothers, monogamy is not required to select for cooperative breeding. Regarding premature helpers, although helping mothers to rear full-sibs will provide double the benefit of those rearing half-sibs, helping to rear half-sibs is still substantially more than zero, the concurrent alternative fitness returns from not helping. Ultimately selection on premature helpers will also depend on whether there are long-term costs. Such costs are seldom considered, although it is noteworthy that contributions to cooperation are condition-dependent [44] and long-term costs can be relatively minor [44,45]. With regard to post-reproductive helpers, whether grandmothers help their grandchildren (r = 0.25) or their own offspring (r = 0.5), their relatedness to those they help is unchanged by the breeding system provided that they direct care to daughters. While we concentrate on premature and post-fertile helpers to make our point, the concept we outline is extendable to any individual in any system with a low chance of currently breeding successfully; potentially including sterile workers in eusocial insects. In cooperative vertebrates, for example, the evolution of cooperative breeding is typically thought to be facilitated by ecological constraints on independent breeding generated by a shortage of vacant habitat of suitable quality [46]. Where constraints are strong enough, a significant number of individuals will never secure a breeding position in their lifetimes, and those that do will tend to be older and/or of high quality. In such circumstances, sexually mature individuals that are relatively young or of low quality could be under selection to help even when their relatedness to recipients is lower than it would be to their own offspring; particularly if mothers are able to coerce such offspring into helping more easily [47,48]. A similar argument might account for the commonly low relatedness coefficients between workers and offspring in many eusocial hymenoptera. Although lifetime monogamy seems to have selected for sterility [8,10], the lack of outside reproductive options for sterile workers might constrain them to now help irrespective of the mating system of their colony [10]. Concluding remarks Recent phylogenetic studies consistently suggest that the evolution of cooperative breeding across taxa has been facilitated by the prior emergence of monogamy. Humans are cooperative breeders, leading to the hypothesis that monogamy evolved during hominin evolution. However, traits typically associated with monogamy are inconclusive in characterizing ancestral mating patterns as being strictly monogamous in hominin. In response, we provide three additional mechanisms that can facilitate kin-selected cooperative breeding in the absence of lifetime monogamy (Box 2). First, although not novel, we remind readers of the potential for kin discrimination to play a key role in the evolution of cooperative breeding. The evidence for indiscriminate help within groups is limited, particularly in cooperative breeders where significant intra-group variation in kinship is common [41]. We suggest that the role of kin discrimination will be particularly efficient in species
Opinion for which any mothers from the same group lay eggs or deliver young separately from others (plural breeding). In such cases, mothers can easily be identified and a single father will ensure that offspring are full-sibs under both monogamy and polygyny. Second, we suggest that birth intervals are a crucial factor in defining relatedness: short birth intervals will increase the probability that offspring can direct care to full-sibs under serial monogamy and polygyny. Consequently, short birth intervals might not only predispose particular species to evolve cooperative breeding, but co-evolve thereafter in response to selection pressure on offspring to help full-sibs. Third, not all offspring have the same outside options regarding their ability to secure fitness directly; most notably, premature and post-fertile individuals cannot gain direct fitness currently and so should be under selection to help individuals of r levels less than 0.5. Most recent forms of the monogamy hypothesis [10] have highlighted the importance of lifetime monogamy in the evolutionary transition to cooperative societies. Lifetime monogamy is possible in hymentoptera because females store sperm for life and males die after mating, and in termites owing to the safe confines in which the king and queen live. In vertebrates, however, the picture is very different, with death, divorce, and usurpation all being commonplace. Whether or not monogamy, when seldom lifetime, provides a universal selection pressure for the evolution of cooperative breeding in such taxa requires further study. In particular, we suggest here that multiple factors can influence relatedness coefficients between successive offspring, and these, in addition to, or instead of, monogamy might have selected for cooperative breeding in some cases. Either way, we suggest that it is important to recognize that, because multiple factors can influence kin structuring and the indirect fitness benefits of helping, future studies need to take a multivariate approach to test whether monogamy is the most important or only factor to select for cooperative breeding in animals for which lifetime monogamy is not feasible. Acknowledgments We thank the Tuesday lunch attendees in Human Evolutionary Biology, Harvard, with whom we had several lively discussions about monogamy and cooperative breeding. We are grateful to Kristen Hawkes, Steve Beckermann, and two anonymous reviewers for their helpful comments on earlier drafts of the manuscript.
References 1 Hrdy, S.B. (2009) Mothers and Others, Harvard University Press, (MA, USA) 2 Russell, A.F. and Lummaa, V. (2009) Maternal effects in cooperative breeders: from hymenopterans to humans. Philos. Trans. R. Soc. B 364, 1143–1167 3 van Schaik, C. and Burkart, J.M. (2010) Mind the gap. Cooperative breeding and the evolution of our unique features. In Mind the Ga (Kappler, P.M. and Silk, J.B., eds), pp. 477–496, Springer 4 Kramer, K. (2011) The evolution of human parental care and recruitment of juvenile help. Trends Ecol. Evol. 26, 533–540 5 Crepsi, B. (2014) The insectan apes. Hum. Nat. 25, 6–27 6 Boomsma, J.J. (2007) Kin selection versus sexual selection why the ends do not meet. Curr. Biol. 17, R673–R683 7 Cornwallis, C.K. et al. (2010) Promiscuity and the evolutionary transition to complex societies. Nature 466, 969–972
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8 Hughes, W.O.H. et al. (2008) Ancestral monogamy shows kin selection in key to the evolution of eusociality. Science 320, 1213–1216 9 Lukas, D. and Clutton-Brock, T. (2012) Cooperative breeding and monogamy in mammalian societies. Proc. R. Soc. B 259, 2151–2156 10 Boomsma, J.J. (2013) Beyond promiscuity: mate-choice commitments in social breeding. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 368, 20120050 11 Russell, A.F. (2004) Mammals: comparisons and contrasts. In Ecology and Evolution of Cooperative Breeding Birds (Koenig, W.D. and Dickinson, J.I., eds), pp. 210–227, Cambridge University Press 12 Clutton-Brock, T.H. (2009) Structure and function in mammalian societies. Philos. Trans. R. Soc. Lond. B 364, 3229–3242 13 Clutton-Brock, T.H. et al. (2002) Evolution and development of sex differences in cooperative behavior in meerkats. Science 297, 253–256 14 Gilchrist, J.S. and Russell, A.F. (2007) Who cares? Individual contributions to pup care by breeders vs non-breeders in the cooperatively breeding banded mongoose (Mungos mungo). Behav. Ecol. Sociobiol. 61, 1053–1060 15 McAuliffe, K. and Whitehead, H. (2005) Eusociality, menopause and information in matrilineal whales. Trends Ecol. Evol. 20, 650 16 Hawkes, K. et al. (1997) Hadza women’s time allocation, offspring provisioning and the evolution of long postmenopausal life spans. Curr. Anthropol. 38, 551–577 17 Kramer, K.L. (2010) Cooperative breeding and its significance to the demographic success of humans. Annu. Rev. Anthropol. 39, 414–436 18 Lahdenpera, M. et al. (2004) Fitness benefits of prolonged postreproductive lifespan in women. Nature 428, 178–181 19 Sear, R. and Mace, R. (2008) Who keeps children alive? A review of the effects of kin on child survival. Evol. Hum. Behav. 29, 1–18 20 Crittenden, A.N. et al. (2013) Juvenile foraging among the Hadza: implications for human life history. Evol. Hum. Behav. 34, 299–304 21 Kramer, K. (2009) Does it take a family to raise a child? In Substitute Parents. Biological and Social Perspectives on Alloparenting in Human Societies (Bentley, G. and Mace, R., eds), pp. 77–99, Berghahn Books 22 Apostolou, M. (2007) Sexual selection under parental choice: the role of parents in the evolution of human mating. Evol. Hum. Behav. 28, 403– 409 23 Beckerman, S. and Valentine, P., eds (2002) Cultures of Multiple Fathers. The Theory and Practice of Partible Paternity in Lowland South America, University of Florida Press 24 Flinn, M.V. and Low, B.S. (1986) Resource distribution, social competition and mating patterning in human societies. In Ecological Aspects of Social Evolution: Birds and Mammals (Rubenstein, B.I. and Wrangham, R.W., eds), pp. 217–243, Princeton University Press 25 Marlowe, F.W. (2000) Paternal investment and the human mating system. Behav. Processes 51, 45–61 26 Murdock, G.P. (1967) The ethnographic atlas. A summary. Ethnology 6, 109–236 27 Walker, R. et al. (2011) Evolutionary history of hunter-gatherer marriage practices. PLoS ONE 6, e19066 28 Kramer, K.L. and Greaves, R.D. (2011) Postmarital residence and bilateral kin associations among hunter-gatherers: pume foragers living in the best of both worlds. Hum. Nat. 22, 41–63 29 Gray, P.B. and Anderson, K.G. (2010) Fatherhood, Harvard University Press 30 Anderson, K.G. (2006) How well does paternity confidence match actual paternity? Curr. Anthropol. 47, 511–518 31 Neel, J.V. and Weiss, K.M. (1975) The genetic structure of a tribal population, the Yanomama Indians. Am. J. Phys. Anthropol. 42, 25–51 32 Kaplan, H. et al. (2000) A theory of human life history evolution: diet, intelligence, and longevity. Evol. Anthropol. 9, 156–185 33 Dixson, A.F. (2009) Sexual Selection and the Origins of Human Mating Systems, Oxford University Press 34 Reno, P.L. et al. (2010) An enlarged postcranial sample confirms Australopithecus afarensis dimorphism was similar to modern humans. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 365, 3355–3363 35 Gordon, A.D. et al. (2008) Strong postcranial size dimorphism in Australopithecus afarensis: results from two new resampling methods from multivariate data sets with missing data. Am. J. Phys. Anthropol. 135, 311–328 36 Lockwood, C.A. et al. (2007) Extended male growth in a fossil sample hominin species. Science 318, 1443–1446
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Opinion 37 Plavcan, J.M. (2012) Implications of male and female contributions to sexual size dimorphism for inferring behavior in the hominin fossil record. Int. J. Primatol. 33, 1364–1381 38 Harcourt, A.H. et al. (1981) Testis weight, body weight and breeding system in primates. Nature 293, 55–57 39 Short, R.V. (1997) The testis: the witness of the mating system, the site of mutation and the engine of desire. Acta Paediatr. Suppl. 422, 3–7 40 Martin, R.D. and May, R.M. (1981) Outward signs of breeding. Nature 293, 7–9 41 Cornwallis, C.K. et al. (2009) Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal. J. Evol. Biol. 22, 2445–2457 42 Lukas, D. and Clutton-Brock, T. (2014) Costs of mating competition limit male lifetime breeding success in polygynous mammals. Proc. R. Soc. B 281, 20140418
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43 Gadagkar, R. (1990) Evolution of eusociality: the advantage of assured fitness returns. Philos. Trans. R. Soc. B 329, 17–25 44 Clutton-Brock, T.H. (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296, 69–72 45 Russell, A.F. et al. (2003) Cost minimization by helpers in cooperative vertebrates. Proc. Natl. Acad. Sci. U.S.A. 100, 3333–3338 46 Koenig, W.D. et al. (1992) The evolution of delayed dispersal in cooperative breeders. Q. Rev. Biol. 67, 111–150 47 Gonzalez-Forero, M. and Gavrilets, S. (2013) Evolution of manipulated behavior. Am. Nat. 182, 439–451 48 Nonacs, P. (2014) Resolving the evolution of sterile worker castes: a window on the advantages and disadvantages of monogamy. Biol. Lett. 10, 20140089 49 Cockburn, A. (2010) Oh sibling, who are thou? Nature 466, 930–931 50 Cockburn, A. et al. (2013) Evolutionary origins and persistence of infidelity in Malurus: the least faithful birds. EMU 113, 208–217
Kin-selected cooperation without lifetime monogamy: human insights and animal implications Karen L. Kramer1,2 and Andrew F. Russell2,3 1
Department of Anthropology, University of Utah, Salt Lake City, UT 84112, USA Department of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA 3 Centre for Ecology and Conservation, College of Life and Environmental Sciences, University of Exeter, Penryn TR10 9FE, UK 2
Recent phylogenetic analyses suggest that monogamy precedes the evolution of cooperative breeding involving non-breeding helpers. The rationale: only through monogamy can helper–recipient relatedness coefficients match those of parent–offspring. Given that humans are cooperative breeders, these studies imply a monogamy bottleneck during hominin evolution. However, evidence from multiple sources is not compelling. In reconciliation, we propose that selection against cooperative breeding under alternative mating patterns will be mitigated by: (i) kin discrimination, (ii) reduced birth-intervals, and (iii) constraints on independent breeding, particularly for premature and post-fertile individuals. We suggest that such alternatives require consideration to derive a complete picture of the selection pressures acting on the evolution of cooperative breeding in humans and other animals. Ancestral mating and contemporary cooperation Humans routinely rely on others to help rear their young, and therefore should be characterized as cooperative breeders [1–5]. Given that cooperative breeding is not shared with other great apes, it was likely derived during hominin evolution. The question is: what facilitated this evolutionary transition in hominin? One hypothesis is that lifetime monogamy favors cooperative breeding because long-term mate-fidelity raises the relatedness among successive siblings to be equivalent to that between parents and offspring [6] (Box 1). Recently, phylogenetic studies have provided compelling evidence that the evolution of monogamous mating patterns preceded the evolution of cooperative breeding across a variety of insect, bird, and mammal species [7–9]. These studies hint that monogamy provides a general rule for explaining evolutionary transitions to cooperative societies (monogamy hypothesis [10]). As such, could the prevalence of cooperative breeding observed in contemporary human societies reflect a monogamous past in hominins? Corresponding author: Russell, A.F. ([email protected]). Keywords: alloparenting; kin discrimination; interbirth intervals; juvenile helpers and grandmothers; mating system; monogamy hypothesis. 0169-5347/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2014.09.001
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We readdress here the question of whether monogamy was prevalent during hominin evolution and, given that the evidence is weak, provide alternative means by which kin-based cooperation could be selected other than through lifetime monogamy. Specifically, we (i) describe cooperative breeding systems in animals, and outline the recent evidence providing general support for the monogamy hypothesis; (ii) highlight that human cooperative breeding systems are not exceptional; (iii) assess the evidence for the monogamy hypothesis in humans using a broad literaturebase; and (iv) provide several alternatives to the monogamy hypothesis for explaining the evolution of kin-based cooperative breeding. We do not attempt an exhaustive review of selection on cooperative breeding; our specific intention is to address whether monogamy was a necessary precondition for cooperative breeding in humans. We find little compelling evidence, and propose that lifetime monogamy is not required to select for cooperative breeding when kin discrimination is likely, birth-intervals are short, and individuals are not currently able to breed independently. Apparent commonalities in cooperative breeders Cooperative breeding describes a system in which individuals help in the reproductive attempts of others. This situation presents a classic evolutionary puzzle because helping should incur a cost to one’s own current or future direct reproductive success. Despite this, cooperative breeding has evolved numerous times within and across diverse taxa including insects, spiders, crustaceans, fish, birds, and mammals [2,10]. Across nonhuman cooperative breeders, individuals who provide care to the offspring of others are usually, but not always, nonbreeders [2,7– 12]. In the hymenoptera (bees, wasps, ants), helpers (or workers) tend to be fertile or sterile adults [8], while in the isoptera (termites) they are often totipotent juveniles [10]. In birds, helpers tend to be sexually mature [2,7], while in mammals premature helpers are common [2,11–14] and post-fertile helpers occur in two whale species [15]. Although variability exists across cooperative breeders in the modes of help provided, status of helpers, group size and mating systems [2,7–12], recent phylogenetically based comparative analyses reveal an apparent commonality
Opinion Box 1. The role of monogamy in selecting for cooperative breeding The strengths of the monogamy hypothesis lie with its simplicity and sound foundation in inclusive fitness theory [6,10]. The inclusive fitness of individuals is governed by their direct + indirect (through collateral kin) genetic contributions to following generations. Consider the general case that each parent can propagate 50% of their genes for any offspring produced. Under monogamy, each offspring produced in a group also shares 50% of its genome, on average, with subsequent offspring in the same group. Thus, where parents are faithful within and between attempts, recruits to the group will be as related to subsequent offspring as they would be to their own. Consequently, at sexual maturity the fitness accruable to previous offspring from helping to rear subsequent offspring coaligns with that of rearing one’s own [relatedness (r) = 0.5 in each case]. This is not automatic under any other mating system (see Table 1 in main text, but see Box 2 for an exception under polygyny). Under all others, female offspring will be more related on average to their own offspring (r = 0.5) than to others produced subsequently in their group (r = 0.25–0.5; less if mothers produce offspring jointly or communally). For male offspring, the story is more complicated because, assuming they know their mother, males can be more related to subsequent offspring produced in the group (r = 0.25–0.5) than they are to their ‘own’ under both polyandrous and promiscuous mating systems (r = 0–0.5). The paradoxical role of high female infidelity on tendencies for sons to cooperate instead of attempt independent breeding has not been addressed. This latter caveat aside, it is easy to see how parental fidelity can have an influential, perhaps defining, role in selecting individuals to stay and help rather than disperse and breed.
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probabilities and extents of help provided by close relatives [20,21]. Given the illuminating results from phylogenetic analyses highlighting the evolutionary relationship between monogamy and cooperative breeding (see above), it is tempting to hypothesize that the prevalence of cooperative breeding in our own species implies a monogamous past.
[10]. First, Hughes et al. [8] conducted a phylogenetic analysis of 267 species of hymenoptera from eight lineages with independent evolutionary origins. Despite variation in modern mating systems (monandry, polyandry, polygyny; see Table 1), they found that monandry was generally the ancestral state to the evolution of cooperative breeding. Second, the importance of monogamy for the evolution of cooperative breeding was replicated in birds. Phylogenetic analysis of 267 bird species showed that cooperative species were threefold less promiscuous on average than noncooperative species [7], and species of non-cooperative ancestors were twice as likely to evolve cooperative breeding if they tended towards monogamy. In a third study, cooperative breeding among mammals was shown to be concentrated in species where females mate exclusively with a single male [9]. In a phylogenetic reconstruction of 1874 mammal species, evolutionary transitions to cooperative breeding were likely associated with monogamy.
Evidence for monogamy in humans? Behavioral evidence: contemporary mating patterns Mating patterns as observed in contemporary small-scale societies, especially hunter-gatherers, which do not have the confounding influences of modern medicine and contraception, are frequently used to make inferences about the past. Across these societies, humans live in multimale– multifemale groups which include multiple breeding females within socially recognized long-term bonds. While such bonds exist in all human societies, these need not be monogamous, and frequently include polygynous and occasionally polyandrous configurations, which vary both within and across societies [22–27]. Although polygynous marriage is sanctioned in 80–85% of traditional human societies [24], this figure is based on cultural norms, not on individual behaviors. Closer scrutiny of these data reveals that cross-sectionally the majority of individuals within a society are currently married monogamously. Notwithstanding, longitudinal data show that men also accumulate wives during their lifetimes and, even where bonds are monogamous, they tend to be serially so in both sexes owing to high mortality and divorce rates, as well as asymmetries in the termination of fertility [25,28]. Paternity outside a pair-bond (promiscuity; but see Table 1 for definitions in cooperative vertebrates) is seldom studied but seems to be limited. A human extra-pair paternity rate of 9% is often quoted, but this study was based on a small number of samples and its design has been critiqued for several reasons [29]. The most thorough cross-cultural study suggests a median nonpaternity rate of 1.7–3.3% depending on sample [30], with the highest known extramarital paternity in a traditional society being about 9% (e.g., the Yanomamo, although estimates vary depending on sampling method) [31]. That humans commonly show paternal care, which also likely evolved following the split from other great apes, is further suggestive of limited promiscuity and strong inter-sexual mate bonds [32].
Cooperative breeding in humans The defining features and characteristics of cooperative breeding introduced above unquestionably apply to modern humans. Across traditional, preindustrial and marketintegrated societies, parents receive substantial, although cross-culturally variable, help particularly from pre-fertile juveniles of both sexes and post-fertile females [4,16]. Help from juveniles and post-fertile females has been shown to have significant consequences for maternal energy expenditure and fitness, primarily through reducing birth intervals and offspring mortality [17–19]. Although humans also are associated with more generalized patterns of cooperation, as in nonhuman cooperative breeders, case studies in traditional human societies reveal preferential
Synthesis Socially monogamous pair-bonds are prevalent in extant human societies, but partners frequently change and any monogamy is often serial (Table 1). In this regard, humans are like all vertebrates but contrast starkly with many cooperative insects which display lifetime fidelity [10]. From the perspective of breeders, the fitness consequences of serial monogamy might differ little from those of lifetime monogamy. However, for a helper the two systems are very different, with serial monogamy equating to polygyny or polyandry when the natal sex is replaced (system depends on which sex is philopatric), and promiscuity when the dispersing sex is replaced (Table 1). In addition, across human societies, a single male is not uncommonly 601
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Table 1. Glossary: mating systems, estimated prevalence in cooperative breeders and outcomes for relatedness among siblingsa Mating system Monandry
Definition Female mates with one male in her life before egg-laying
Example systems Many hymenopteran insects
Monogamy
One female pairs with one male (social) or mates with one male (genetic) One female mates with > 1 male (vertebrates: includes only withingroup males)
Termites, most birds, many mammals including humans
Polyandry
Polygyny
Hymenoptera: > 1 queen per colony; others: 1 male mating with >1 female within the group
Promiscuity
Female infidelity arising with males outside the pair-bond (humans) or outside the group (other animals) Identity of partner changes between reproductive events, through death, divorce, usurpation
Between-attempt infidelity (e.g., serial monogamy)
Common in advanced eusocial hymenoptera; relatively common in birds, fish, and mammals; exceptional in humans Common in hymenoptera, occurs birds and mammals, including humans
Common in birds, occurs in mammals and humans All vertebrates, including humans
General outcome All offspring born during the life of a queen have the same parents; the genes of the sire die with queen. Depends on infidelity: in termites infidelity is exceptional, in mammals it is low and in birds it is highly variable (see below). Depends on male–male relatedness (r): 0 in eusocial insects, generally high in mammals, and variable in birds. All else being equal, leads to among-sibling r values of 0.25–0.5. Polygyny dilutes group r values. Consequences depend on kin discrimination [easy if mothers clutch/birth at different time or place (plural breeding; among-sib r = 0.5); but not if same time or place (communal/joint-nesting, among-sib r = 0.25–0.5 – same father but different multiple mothers]. Depends on level of infidelity, but will push among-sibling r levels closer to 0.25 because fathers will tend to be unrelated. Potentially dramatic: even assuming withinattempt monogamy – replacement of the natal versus dispersing sex leads to r values between successive offspring of 0.25–0.375 and of 0.25, respectively.
a
Note that definitions are presented as applied to cooperative breeders, and may or may not be generalizable to other systems.
bonded with multiple females at some point in his life (simultaneous polygyny). Thus both serial monogamy and polygyny represent common mating patterns in humans; the relative importance of each during our evolutionary history is difficult to assess. Although mating patterns in contemporary societies are often used as analogies to the past, the diversity we see today might be evolutionarily derived following migration into new and contrasting ecologies [7–9]. Consequently we turn to anatomical signatures of ancestral mating patterns. Morphological evidence: sexual size dimorphism and testis size Anatomical traits, being less plastic than behavioral ones, take longer to modify following a change in selection pressure. As such, current morphology can be integrated with fossil evidence to elucidate evolutionary responses to ancestral selection pressures. Below we consider two morphological traits commonly used to make inferences about past mating patterns: sexual size dimorphism and primary sexual traits in the form of testis size. Sexual dimorphism Modern human body size dimorphism is relatively modest, slightly greater compared to other monogamous primates, but much less compared to polygynous species [33]. In fossil specimens, the general consensus has been that stature dimorphism was greater in the past and has diminished during hominin evolution, suggesting a decline in male–male competition. Some argue that size dimorphism in australopithecines was sufficiently attenuated to suggest an early monogamous and male provisioning ancestor [34]. Others are persuaded that the level of skeletal 602
dimorphism in australopithecines was sufficiently dimorphic [35] to suggest a male reproductive strategy focused on monopolizing females [36]. In light of these conflicting views, Plavcan [37] cautions that, although dimorphism indicates some degree of male agonistic competition, it is not a reliable indicator of mating behavior in extinct species. All that we can say for apparent certainty is that, if our last common ancestor were ‘gorilla-like’, we have become less dimorphic and less polygynous, and if it were ‘chimp-like’ we have maintained levels of dimorphism but have become less promiscuous. Either way, it is not clear from the sexual size dimorphism evidence that humans were ever fully monogamous. Testis size Sperm competition, associated with polyandrous or promiscuous matings, should be manifest in large testes relative to body size [38]. Humans have slightly smaller testes than predicted from body size, suggesting low female promiscuity [39]. Adjusting for body size, human testes are considerably smaller than those of chimpanzees, suggesting selection against female promiscuity, but somewhat larger than other monogamous primates [38]. A recent reanalysis, including a broader spectrum of populations, shows that humans encompass the range of variation for polygynous gorillas and orangutans, but not promiscuous chimpanzees, which is consistent with pair-forming polygynous or (serially) monogamous species [33]. While testis size is a predictor of female promiscuity, it is often mistakenly used as an indicator of monogamy. However, it cannot discriminate between monogamy and harem-based polygyny because in both cases sperm competition is expected to be relatively low [33,40].
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Box 2. Empirical shortcomings with the monogamy hypothesis and directions for future research There are three problems for the monogamy hypothesis when applied to vertebrates and some invertebrates. (i) The lack of compelling evidence for a monogamous past in hominin is not exceptional: phylogenetic analyses also suggest that monogamy did not precede cooperative breeding in a notable number of extant bird species [49]. (ii) While the phylogenetic analyses in birds also showed that an evolutionary history of promiscuity has selected against cooperative breeding in a significant number of cases, there are again important exceptions. For example, Australian fairy-wrens are one of the most promiscuous species so far documented, but most (if not all) remain cooperative breeders [50]. (iii) While individuals breed monogamously, no vertebrate species is lifetime monogamous; mortality, divorce, and usurpation are common. Thus, other factors clearly select for kin-selected cooperative breeding, and the question is what are they? Below we set out the more salient and testable additional (or alternative) hypotheses to the monogamy hypothesis for species lacking lifetime monogamy, while maintaining the theme of a general role of relatedness. Note that mating systems include serial scenarios (i.e., between-attempt infidelity; see Table 1 in main text). Hypothesis Kin discrimination allows cooperative breeding to evolve under alternative mating patterns Plural breeding increases scope for kin discrimination; hence cooperative breeding
Rationale/explanation First-order relatives can be helped under polygyny when mothers can be identified (see Table 1 in main text and below) Where eggs/offspring are delivered in different locations, bonds between mother and offspring will arise
Reduced birth-intervals increases relatedness among successive sibs
Vertebrates are prone to infidelity through partner loss; reduced birth intervals will mitigate this Low opportunity costs; relatedness to those they help exceeds 0 (0.25–0.5), regardless of mating system No individual is equal and many offspring fail to secure reproductive positions in life
Juvenile and post-fertile helping can be selected without monogamy Reduced outside reproductive options for fertile individuals will increase selection for helping lower orders of relatives High promiscuity selects for male helpers
Sons are often more related to mother’s offspring than to their ‘own’
Synthesis Several lines of morphological evidence appear to rule out strong promiscuity or polyandry in our recent past, but are unable to distinguish between monogamy and polygyny, or the extents and patterns of serial monogamy. The bestsupported conclusion seems to be that monogamy is firmly within, but not exclusive to, the repertoire of human mating strategies. Nevertheless, there is ambiguity about its time-depth, whether it relates to the evolution of cooperative breeding, and whether inter-sexual bonding developed in the context of a polygynous or monogamous breeding system. Because evidence can be found to characterize human breeding systems in a variety of ways, we caution against definitive views that rally partial evidence to forward particular perspectives. Cooperative breeding without (lifetime) monogamy The evidence for hominins passing through a monogamy bottleneck and emerging as a cooperative breeder is not particularly strong. This leads to two related questions. First, is the comparative evidence from other vertebrates sufficiently compelling to convince us that humans must have had a monogamous past, irrespective of the evidence? Second, are there alternative routes to kin-selected cooperative breeding other than through the evolution of monogamy? Below we focus on the latter and propose three main alternatives to the model that a monogamous past is a necessary prerequisite for the evolution of cooperative breeding through kin selection (Box 2). Our aim is not to undermine a facilitating role of monogamy in the evolution of cooperative breeding, but to illustrate that additional
Appropriate model systems Vertebrate species showing polygyny
Many species: plural breeding is more common than accredited, and is often confused with communal breeding where females deliver simultaneously in the same place All species: key unanswered question – how do ancestral birth intervals predispose species to cooperation? Mammals including humans; eusocial insects
All species: key unanswered question – how does probability of breeding at a given age or level of condition relate to selection for cooperation? Birds: promiscuity common
(or alternative) mechanisms can enable kin-selected cooperative breeding in the absence of lifetime monogamy (Box 2). Kin discrimination A benefit of lifetime monogamy in selecting for cooperative breeding is that all successive siblings are always related by an equivalent to one’s own offspring (Box 1). Kin discrimination reduces a requirement of (lifetime) monogamy in the evolution of cooperative breeding through kin selection because it allows offspring to help only when close-kin are available. Comparative analysis in cooperative birds shows that kin discrimination is an important mechanism ensuring kin-biased cooperation in groups where individuals vary in relatedness [41]. Whether or not kin discrimination can offer a suitable alternative selective force for cooperative breeding in the absence of lifetime monogamy depends on several other factors. For example, consider a group of animals where multiple females lay eggs or deliver live offspring simultaneously in the same nest or burrow (i.e., so-termed joint-nesting or communal breeding). The ability of offspring to recognize their mother will be near impossible in the egg-laying scenario and challenging in the viviparous one. By contrast, identifying mothers become significantly more efficient if multiple mothers in the same group breed plurally; in other words, in a different location or time, as is the case in humans. Under plural breeding, it is irrelevant whether or not each female has her own mate (monogamy) or shares a mate with other females (polygyny), because in both cases successive sibs have the same parents and will be as related to each other 603
Opinion as to their own offspring (assuming no parental death). While male tenure lengths are reduced in polygynous species compared with monogamous ones, in most cases males still survive successive births [42], allowing many offspring to direct care towards full siblings. Thus, all else being equal, monogamy need not elevate relatedness among successive sibs any more than polygyny provided that mothers can be reliably identified and fathers survive to sire successive births. Interbirth intervals In great apes, the likelihood that successive siblings will be related is partially reduced by the length of birth intervals. Because birth intervals are long (4–8 years), they often exceed the tenure of the dominant male and, regardless of breeding system, negatively affect the probability that successive offspring will be full siblings. Relative to the great apes, humans have considerably shorter birth intervals, which, in conjunction with the fact that helpers in humans are often subadults (see below), increases the probability that full-sibs can be helped under polygyny or serial monogamy. Whether or not species with short birth intervals are more likely to evolve cooperative breeding has not been tested. It is at least noteworthy that cooperative birds are most prevalent in Australia and Africa where selection to breed repeatedly within short and unpredictable rains is often intense. Although reduced birth intervals are generally thought of as being a consequence, rather than a cause, of cooperative breeding, the near ubiquity of this helper effect across cooperative societies is intriguing. One possibility is that reduced birth intervals are partly selected by parent(s) maximizing the probability that successive siblings are first-order relatives and hence that they receive maximal help with offspring care. We hypothesize that short birth intervals will facilitate the evolution of cooperative breeding and, following its evolution, be under selection to shorten further to capitalize on kin-biased helper investment strategies. Premature and post-fertile helpers The role of monogamy in the evolution of cooperative breeding might depend on the status of predominant helper types. For sexually fertile individuals, the fitness incentive to delay reproduction and help might be low where potential recipients have a relatedness (r) of less than 0.5 (Box 1 and Table 1), although this will be condition- or quality-dependent (see below). By contrast, for the premature (e.g., juvenile or sub-adult age classes) or post-fertile (e.g., grandmothers), no scope for accruing current direct fitness exists. For the former, helping provides an opportunity to gain immediate indirect fitness [43], which might have negligible detriment to future direct fitness, particularly given a significant time-frame to recoup any costs (see below). For the latter, helping represents the only way to gain any further fitness. As such, for each, we might expect that r levels below 0.5 between donor and recipient are sufficient to select for cooperative breeding. In birds, premature helpers are uncommon and seldom effective, while post-fertile helpers are not known. By contrast, in mammals, premature [11–14] helpers can represent a significant part of the workforce for many 604
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species, as do post-fertile helpers in some cases [15]. The key point we wish to make here is that for both juveniles and grandmothers, monogamy is not required to select for cooperative breeding. Regarding premature helpers, although helping mothers to rear full-sibs will provide double the benefit of those rearing half-sibs, helping to rear half-sibs is still substantially more than zero, the concurrent alternative fitness returns from not helping. Ultimately selection on premature helpers will also depend on whether there are long-term costs. Such costs are seldom considered, although it is noteworthy that contributions to cooperation are condition-dependent [44] and long-term costs can be relatively minor [44,45]. With regard to post-reproductive helpers, whether grandmothers help their grandchildren (r = 0.25) or their own offspring (r = 0.5), their relatedness to those they help is unchanged by the breeding system provided that they direct care to daughters. While we concentrate on premature and post-fertile helpers to make our point, the concept we outline is extendable to any individual in any system with a low chance of currently breeding successfully; potentially including sterile workers in eusocial insects. In cooperative vertebrates, for example, the evolution of cooperative breeding is typically thought to be facilitated by ecological constraints on independent breeding generated by a shortage of vacant habitat of suitable quality [46]. Where constraints are strong enough, a significant number of individuals will never secure a breeding position in their lifetimes, and those that do will tend to be older and/or of high quality. In such circumstances, sexually mature individuals that are relatively young or of low quality could be under selection to help even when their relatedness to recipients is lower than it would be to their own offspring; particularly if mothers are able to coerce such offspring into helping more easily [47,48]. A similar argument might account for the commonly low relatedness coefficients between workers and offspring in many eusocial hymenoptera. Although lifetime monogamy seems to have selected for sterility [8,10], the lack of outside reproductive options for sterile workers might constrain them to now help irrespective of the mating system of their colony [10]. Concluding remarks Recent phylogenetic studies consistently suggest that the evolution of cooperative breeding across taxa has been facilitated by the prior emergence of monogamy. Humans are cooperative breeders, leading to the hypothesis that monogamy evolved during hominin evolution. However, traits typically associated with monogamy are inconclusive in characterizing ancestral mating patterns as being strictly monogamous in hominin. In response, we provide three additional mechanisms that can facilitate kin-selected cooperative breeding in the absence of lifetime monogamy (Box 2). First, although not novel, we remind readers of the potential for kin discrimination to play a key role in the evolution of cooperative breeding. The evidence for indiscriminate help within groups is limited, particularly in cooperative breeders where significant intra-group variation in kinship is common [41]. We suggest that the role of kin discrimination will be particularly efficient in species
Opinion for which any mothers from the same group lay eggs or deliver young separately from others (plural breeding). In such cases, mothers can easily be identified and a single father will ensure that offspring are full-sibs under both monogamy and polygyny. Second, we suggest that birth intervals are a crucial factor in defining relatedness: short birth intervals will increase the probability that offspring can direct care to full-sibs under serial monogamy and polygyny. Consequently, short birth intervals might not only predispose particular species to evolve cooperative breeding, but co-evolve thereafter in response to selection pressure on offspring to help full-sibs. Third, not all offspring have the same outside options regarding their ability to secure fitness directly; most notably, premature and post-fertile individuals cannot gain direct fitness currently and so should be under selection to help individuals of r levels less than 0.5. Most recent forms of the monogamy hypothesis [10] have highlighted the importance of lifetime monogamy in the evolutionary transition to cooperative societies. Lifetime monogamy is possible in hymentoptera because females store sperm for life and males die after mating, and in termites owing to the safe confines in which the king and queen live. In vertebrates, however, the picture is very different, with death, divorce, and usurpation all being commonplace. Whether or not monogamy, when seldom lifetime, provides a universal selection pressure for the evolution of cooperative breeding in such taxa requires further study. In particular, we suggest here that multiple factors can influence relatedness coefficients between successive offspring, and these, in addition to, or instead of, monogamy might have selected for cooperative breeding in some cases. Either way, we suggest that it is important to recognize that, because multiple factors can influence kin structuring and the indirect fitness benefits of helping, future studies need to take a multivariate approach to test whether monogamy is the most important or only factor to select for cooperative breeding in animals for which lifetime monogamy is not feasible. Acknowledgments We thank the Tuesday lunch attendees in Human Evolutionary Biology, Harvard, with whom we had several lively discussions about monogamy and cooperative breeding. We are grateful to Kristen Hawkes, Steve Beckermann, and two anonymous reviewers for their helpful comments on earlier drafts of the manuscript.
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