Sex-ratio conflicts, kin selection, and the evolution of altruism

Wladimir J. Alonso* and Cynthia Schuck-Paim

Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, United Kingdom

Edited by Edward O. Wilson, Harvard University, Cambridge, MA, and approved March 6, 2002 (received for review November 1, 2001) Kin-selection theory has thrived in the explanation of a wide several individuals, functioning at a new level of selection (the variety of biological phenomena, chiefly the evolution of biological eusocial colony). altruism as that found in sterile castes of eusocial insects. Much of Nowadays some kin-selection defenders support the idea that the way in which it has been tested is based on the existence of the two theories are complementary, and that in fact the role of conflicts over sex-ratio production within eusocial colonies. How- manipulation is to create better conditions for the fixation of the ever, despite neatly showing eusocial colonies as arenas where altruistic gene (9, 18). Although the idea is consistent with selection at the gene level triggers the appearance of sophisticated the internal logic of kin-selection theory, it leaves unanswered disputes, these studies have only demonstrated the existence of the question of when, during the evolution or development of a genes that act by biasing sex ratios to promote their own spread. eusocial colony, it would be unequivocally necessary to invoke Here we argue that such genes depend on the social organization the existence of a kin-selected altruistic gene. Crozier (18) of the colonies where they are expressed, but that they are not, proposes that a ‘‘nonresponse to manipulation’’ could be con- in any way, the precursors of these societies—the major implica- sidered as an altruistic gene in the kin-selectionist sense. The tion being that unequivocal evidence that eusociality evolved argument, however, is not helpful for the identification and through the action of kin-selected altruistic genes is still lacking. description of evolutionary innovations, as in that same line of Additionally, we highlight the neglect of alternative theories reasoning (and so playing the game of working in an ‘‘all is on the explanation of both biological altruism and sex-ratio con- adaptive’’ world) that lack of response could be also regarded as flicts, and defend that the enthusiasm with the latter has, in some an adaptation of the new level of organization represented by the cases, led to its inappropriate use as a basis for the explanation colony. It has been also postulated that what we sometimes see of other biological characteristics of eusocial organisms, when as manipulative devices in eusocial colonies (such as pheromonal accounts based on phylogenetic or physiological constraints are control and aggressive interactions) would in fact be signals to also available. allow those individuals possessing the altruistic gene to decide whether or not to help the signaling party (19–21). The fact that the manipulation could operate through signals more than ver since its formulation in 1963 by William Hamilton (1–4), through direct inhibitors is also accommodated by the logic of Ekin-selection theory has flourished in the prospect of ex- the manipulation theory: efficient communication systems are plaining a wide range of sophisticated patterns of animal be- expected to evolve inside an organism (as a eusocial colony can havior, being often regarded as one of the most (or even the be considered) once it has been already established, replacing most) important evolutionary insights of the recently finished the direct inhibition systems that once allowed its formation. In century (5). Among its greatest contributions is the formulation fact, indirect and ritualized forms of communication are ob- of an evolutionarily acceptable framework for the appearance served predominantly in highly eusocial organisms, whereas in and maintenance of the so-called biological ‘‘altruism,’’ through primitively eusocial societies, dominant individuals rely on more which individuals behave by lowering their own potential for direct forms of aggression (7, 8, 13). reproduction or survival in favor of the reproduction of other Although it is not our aim to defend one theory against the individuals of the same species. other, it is necessary to mention that the main argument broadly A central problem addressed under the theory’s scope is the used to undermine manipulation theory (9, 22) in fact does not evolution of sterile castes of workers in colonies of eusocial (6–8) affect it. The argument is based on the analysis of the viability organisms, such as ants, termites, and some bees and wasps. of a eusocial system evolving through the manipulative route According to the theory, the evolution of worker castes was when strategies of resistance to manipulation arise in the ma- possible only because of the success of genes (hereafter ‘‘altru- nipulated individuals.† As any genetic system, a eusocial colony istic genes’’) codifying for behaviors whereby their carriers is certainly exposed to disruption of its organization due to the sacrifice their own reproductive output by helping the repro- invasion of selfish strategies among the lower levels of organi- duction of individuals who most likely have these genes. The zation, and as so only those systems able to cope with it through conditions for these genes to spread are given in the well-known the fixation of compensatory or suppressor strategies (see below) Hamilton rule (9): rb Ϫ c Ͼ 0, where r is the coefficient of kinship will be able to survive. An invasion by selfish or opportunistic between the altruist and the receiver of the altruism, b is the benefit in terms of extra offspring for the receiver of the altruistic This paper was submitted directly (Track II) to the PNAS office. act and c is the cost for the altruist’s offspring production. Abbreviation: SGE, selfish genetic element. An alternative explanation for the emergence and evolution of sterile castes in eusocial organisms states that the characteristic *To whom reprint requests should be addressed. E-mail: [email protected]. (or ‘‘gene,’’ in the present operational language) under selection †An influential argument against parental manipulation was that put forth by Dawkins (9, 23), who argued that the expression of a gene by a parent against the interests of an is one that imposes the nonreproductive role to part of the brood, offspring would be counterselected through this parent having also been part of a by handicapping its full reproductive development through a manipulated offspring. The argument, however, misses the important point that the shortage of resources and͞or agonistic interactions [‘‘parental- parent in question is exactly the reproductive (favored) part of the manipulated offspring. The manipulation was directed only against those individuals converted into helpers, not manipulation theory’’ (10, 11); see also refs. 12–17]. As a result, against this parent. the eusocial system would not emerge because of the expression The publication costs of this article were defrayed in part by page charge payment. This EVOLUTION of altruistic genes, but instead because of the evolutionary article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. advantage provided by a developmental process comprising §1734 solely to indicate this fact.

www.pnas.org͞cgi͞doi͞10.1073͞pnas.092584299 PNAS ͉ May 14, 2002 ͉ vol. 99 ͉ no. 10 ͉ 6843–6847 Downloaded by guest on September 28, 2021 strategies is certainly also a ‘‘problem’’ that a colony evolving to kin selection by Trivers and Hare (33). As mentioned, through kin selection would have to face. Kin selection ‘‘solves’’ altruistic genes should make their bearers benefit preferentially this problem simply by imposing in its basic formulation (Ham- the class of individuals who most likely share the same genes to ilton’s rule, above) that the overall genetic benefit for the promote their spread. In monogynous hymenopteran societies altruistic gene has to be positive so that the altruistic behavior headed by a single-mated queen, workers are highly related to can spread. If we follow the same line of reasoning, manipulative their sisters, and would pass on their genes three times more genes could also just demand a beneficial outcome for the spread efficiently through sisters than through brothers. The queen, on of manipulative actions. The argument therefore does not pro- the other hand, has the same degree of relatedness with both vide useful insights as to which theory better explains the sons and daughters. Following this logic, Trivers and Hare (33) evolution of altruism in eusocial colonies. That is why it is proposed that conflicts of interests over sex ratios should exist important to clearly establish in which aspects the theories can between the queen and her worker progeny, because while be really distinguished and tested. workers would be interested preferentially in the production of In fact, if kin-selection literature is carefully scrutinized, one females, the queen should be interested in the maintenance of a can notice that several of the studies designed to test the role of Fisherian 1:1 ratio among its reproductive brood. Support for the kin selection on the evolution of eusociality are not comparisons theory would therefore come if individuals behaved by biasing of its predictions against those of other hypotheses, but solutions the sex ratio in accordance to their genetic interests. From the to the problems that the acceptance of kin selection itself poses. same perspective, a diverse set of predictions can be derived if For instance, Queller (23) states that a prediction of kin selection the genetic structure of the colony and population increases in is that ‘‘colony mates must be related and that sterility must be complexity, which may happen because of the presence of conditionally expressed.’’ Because those are well-established several queens in a colony, multiple mating, and͞or reproduction facts, this theory would be strongly supported. However, the of the workers (9, 20, 23–25, 29–31). conditionality of the worker–queen trait is not a prediction of kin Within this theoretical framework, a number of studies have selection, but simply an aspect of the generation of division of shown eusocial colonies as arenas where the selection at the gene labor inside the colony that any theory should explain, and not level triggers the appearance of sophisticated disputes aimed at restate as a prediction. In the same way, the search for higher one’s own genetic overrepresentation. Nevertheless, a closer degrees of relatedness is not a test against manipulation theory, analysis reveals the limitations of the potential of such genes in for this theory too is based on a process that takes place within the evolution of eusociality. To illustrate this, we examine some the same familiar brood (so that the developmental mechanism representative examples selected from the vast literature on the under selection can be passed on to the next generation). In fact, subject. To avoid personal bias, we use the same selection as that it is only a search for the conditions for the fixation of the used in a recent paper (24) aimed at explaining the success of altruistic gene, and as such, an internal problem for kin selection kin-selection theory based on studies of social conflicts in [that is, finding the conditions foreseen by this theory does not eusocial insects. necessarily imply the existence of kin-selected altruistic genes, it Sundstrom et al. (34) found that workers of the wood ant only implies that the conditions exist for them to be fixed (12)]. Formica exsecta were killing the male larvae in single-mated Yet, quantitative tests of Hamilton’s rule have not proved an queen colonies, but not in multiple-mated queen colonies. The easy task (23–28). As pointed out by Bourke (24), attempts to behavior can be thus interpreted in accordance with the Trivers accurately measure offspring numbers gained and lost through and Hare (33) model, because in the former case workers would altruism have met many obstacles. Additionally, it has been prefer to raise sexual females, to whom they share a higher shown that, owing to the occurrence of competition between degree of relatedness, instead of males. In the latter case, relatives, estimates of even high degrees of relatedness are not however, the interest of workers over the sex ratio would sufficient evidence for the role of kin selection in promoting coincide with that of the queen–and so they should rear all brood altruism (27, 28). produced. Another example that is presented as ‘‘explained by kin Sex-Ratio Conflicts and Eusociality selection and by no other theory’’ (24) is the case of worker Given the difficulties previously mentioned, one of the predom- policing (35–38). It states that workers in haplodiploid colonies inant ways of testing the theory has been the investigation of its should be selected to allow—or instead ‘‘police’’—the process of predictions regarding the existence of sex-ratio conflicts within egg laying by other workers depending on the degree of relat- societies (9, 20, 23–25, 27, 29–31). As Chapuisat and Keller (25) edness among the workers, and among the workers and the highlight, ‘‘empirical tests of kin selection have proved difficult, queen(s). In single-queen, single-mated colonies workers would because social behavior has been shaped by the interaction of be more related to each others’ sons than to the queen’s sons, and multiple ecological and genetic factors over evolutionary time. therefore allowed to lay the unfertilized, male-producing eggs. In Studies of sex allocation in hymenopteran societies have polygynous or multiple-mated queen colonies, however, workers emerged as prime tests of kin selection because sex-allocation would benefit by suppressing each other’s egg laying in favor of theory provides quantitative predictions based on variation in the queen’s male offspring. Within this perspective, Foster and relatedness.’’ Indeed, the outcome of such tests has been seen as Ratnieks (39) studied the social wasp Dolichovespula saxonica,a extremely favorable, as Queller and Strassmann (31) point out: model species for testing the worker-policing hypothesis as the ‘‘the most striking support for kin-selection theory from any mating frequency of single queens present in each colony varies organism comes from studies of sex ratios.’’ among colonies. They indeed confirmed the outlined prediction: However, here we argue that because altruism is not involved in single-mated queen colonies the proportion (70%) of male in these conflicts, the approach gives only limited support for the eggs reaching adulthood did not differ between those produced role of kin-selected genes on the evolution of eusociality. We also by workers and by the queen. On the other hand, in multiple- remark the existence of alternative theories for the phenomena, mated queen colonies only 10% of the male eggs laid by workers and finally we highlight that explanations based on the occur- reached adulthood (as opposed to 75% laid by the queen). rence of sex-ratio conflicts have been frequently overused when However, a closer analysis of these examples and others simpler explanations based on an organism’s life history or involving sex-ratio conflicts shows us a common denominator in phylogenetic constraints are also available. the behavior of workers: the individuals performing these acts Kin-selection predictions’ on sex-ratio conflicts were devel- are not paying any cost in terms of Darwinian fitness by behaving oped from the application of the sex-ratio theory of Fisher (32) in those ways. We could describe the action of the genes involved

6844 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.092584299 Alonso and Schuck-Paim Downloaded by guest on September 28, 2021 as codifying the following instructions in workers: in the first Needless to say, we do not claim that all conflicts over sex example ‘‘kill brothers when you are daughter of a single-mated ratios should be interpreted under the SGE framework. How- mother,’’ and in the second example ‘‘kill workers’ eggs when you ever, it is our aim to highlight that plausible alternative expla- are daughter of a single-mated mother.’’ Yet, although the nations exist (see also ref. 17 for a review of alternative models codified behaviors indeed favor the spread of copies of the genes of sex allocation in primitively social bees) to phenomena promoting them, they do not bear any direct fitness cost to traditionally viewed under the exclusive approach of kin performers or can be thought of as the ones that could have led selection. them into a sterile condition. As previously exposed, kin selec- tion was presented as a novelty because it would explain the Sex-Ratio Conflicts and Social Biology of Organisms evolution of altruistic behaviors, and among all of the definitions It has been increasingly common to attempt explaining several for biological altruism, at least it is agreed that the individual has aspects of the social biology of eusocial colonies as shaped by to suffer a loss in either its direct reproduction or survival when conflicts over sex ratios. Contrary to this approach, we argue that performing the altruistic act. To test the theory as an explanation the analysis of social traits as by-products of sex-ratio conflicts for eusocial evolution it is thus not sufficient to show that there has been frequently overused when simpler explanations based are genes or strategies that at no cost, and making profit of an on an organism’s life history or phylogenetic constraints are also already established social organization, can promote their own available. As a representative example we analyze the work of spread by distorting sex ratios. Peters et al. (55) on stingless bees (Meliponini), in which the Additionally, once it is considered that the behaviors per- authors confirm previous suggestions that single-mating is wide- formed by workers in sex-ratio conflicts bear no cost in the sense spread in this group, as opposed to the multiple-mating system previously defined, the use of Hamilton’s rule is not essential to of honeybee queens. Because of the sex-ratio conflicts predicted understand the phenomena. For example, when the eusocial for single-mating systems, stingless-bee workers should be in colony is functionally and evolutionarily regarded as an organism direct competition with the queen. From this principle, the or ‘‘superorganism’’ and thus as a unit of selection (9, 23, 40–42), authors take a further step in deducing the explanation of a series and it is acknowledged that selection can take place at many of biological traits particular to the group. interacting levels (with some genes, as another unit of selection, For instance, they advocate that the ritualized agonistic be- behaving selfishly to promote their overrepresentation), it seems haviors observed during the cell provisioning and oviposition simpler to understand the phenomena by considering the sex- process actually reflect the predicted existence of conflicts ratio-distorter strategies found in eusocial colonies as analogs to between workers and queens. However, a closer look at the the strategies used by some genes in conflicts emerging inside the biology of this group reveals fundamental differences in the way genome of individual organisms. These ‘‘selfish genetic ele- provisioning is performed (7, 56–58) as compared with that seen ments’’ (SGEs), as they are defined, have been demonstrated to in honeybees. Stingless bees mass provision the brood cells act in organisms in several, and even dramatic, ways (43–46). before oviposition. The process can be highly variable between They are vertically transmitted as genetic entities that manipu- species but, as opposed to the process in honeybees, it usually late their ‘‘host’’ to promote their own spread, usually at a cost demands a quick and continuous communication between the to other genes within the genome. In the case of social insects, queen and workers so that all of its steps (e.g., signaling, SGE frequency could be increased as a result of a differential provisioning, and sealing of the cell) can be properly accom- expression according, for example, to the caste of the individual plished. A highly efficient and intense communication system is host. While in queens these units can spread directly through thus required, and it seems difficult to imagine another way it reproduction, for example, in workers a transmission advantage could operate other than through direct interactions between the could be achieved through the expression of traits causing the parties, benefiting from a preexistent behavioral repertoire. death of (or spiteful behavior toward) individuals lacking copies In the same way, the fact that workers and males are reared of them. in identical cells (contrary to Apis) is explained as a mechanism The presence of SGEs also sets the context for the emergence that evolved in this group to avoid conflicts ‘‘because male eggs of conflicts, as they make possible the spread of other genes laid in identifiable cells would be more easily removed by the (referred to as ‘‘suppressors,’’ see ref. 43) with opposite effects opposing party.’’ However, the argument misses the very point in the same organism. Because of their higher genetic diversity, that the evolutionary innovation of having different cell types for colonies with several and͞or multiple-mated queens are partic- rearing males and females belongs to Apis, and Meliponinae only ularly exposed to invasion by some patri- or matriline- retains an ancestral feature, in which the mother (and in some transmitted SGEs that can cause those workers inheriting them cases the reproductive workers) decides the ploidy of the egg, to behave ‘‘parasitically’’ by laying eggs and helping less in colony regardless of the cell type. Additionally, the explanation does not tasks (this has been found, for instance, in some strains of honey address the really interesting innovation inside one of the bees; refs. 47 and 48). Therefore, the fixation of suppressor stingless-bee groups, that is the fact that in the Melipona genus strategies (worker policing in this case) could be explained all cells (not only for males and females, but also for queens and simply as a mechanism of conflict control by the colony to avoid workers) are identical. If cells were identical to avoid the removal that kind of parasitism. In fact, a ‘‘colony-level benefit’’ argu- of male larva, why then would the cell of a queen be also ment is the one that many authors use in those cases where the identical, if workers are not interested (as they argue) in existence (or absence) of worker policing contradicts kin selec- eliminating the excess of queens? tion predictions (49–51). Foster and Ratnieks (52) themselves The tolerance of workers toward virgin queens in the stingless- apply it for Vespula vulgaris, when finding worker policing but bee nest is also explained from kin selection’s standpoint, failing to find evidence that workers were more related to the because of their high degree of relatedness. It also seems simpler queen than to each other, or when finding worker policing in to acknowledge the fact that, given the complete sealing of the colonies with low effective paternity, in which workers of Vespa cell after the egg is laid, it is not possible to rear gynes in crabro were killing their closer relatives to favor more distant queenless colonies, and so there is always the need to maintain ones (53, 54). In these cases, they consider that the worker a stock of virgin queens to ensure the perenniality of the colony policing behavior ‘‘may be selected due to the colony-level (7, 56, 59). Peters et al. (55) are contrary to this alternative benefit of conflict suppression.’’ As we have just described, the explanation for believing that the sealing of the cell would not EVOLUTION rationale applies not only to V. vulgaris and V. crabro, but to in reality be a constraint, as ‘‘in some species microqueens can D. saxonica as well. emerge from worker cells, while in others, a worker larva can

Alonso and Schuck-Paim PNAS ͉ May 14, 2002 ͉ vol. 99 ͉ no. 10 ͉ 6845 Downloaded by guest on September 28, 2021 become a queen by chewing into another cell to gain extra food.’’ organization. Actions described in sex-ratio conflicts cannot be However, the argument is not valid, because, apart from being attributed to genes that act at the expense of direct reproduction. restricted to a small group of species with different evolutionary On the contrary, genes involved in those conflicts could be histories within the stingless-bees’ group, it also fails to appre- referred to as ‘‘parasites’’ of social colonies, not as their ciate the fact that the production of microqueens or queens from ‘‘promoters.’’ worker cells is not triggered for the replacement of a queen Besides kin selection, there are other candidate models for the exactly when it dies (we see no means how it could be), and thus emergence and evolution of eusocial colonies as previously cannot be a mechanism to ensure the perenniality of the colony mentioned (10, 11). From an alternative perspective, reproduc- without the constant maintenance of a virgin queen stock. tive altruism is not a product of selective pressures acting on Conclusion genes contained in altruistic individuals. Conversely, the viability of an organism composed of subunits (like a multicellular Hamilton’s rule provided a general framework for the under- individual, or a eusocial colony) is viewed as largely conditioned standing of the evolution of altruism by determining the condi- on the suppression (and not action) of the ‘‘reproductive inter- tions whereby actions causing an individual to behave to its own est’’ of the lower components. Selection on these higher levels of detriment would spread to fixation. Resulting from this would be the onset of eusociality, and in the same way the evolution of organization would basically act on the mechanisms allowing an some other major biological transitions, chiefly the division of unequal distribution of phenotypes among a genetically homog- labor in multicellular organisms. Empirical tests of the rule have enous brood to be canalized for the generation of a coordinated nonetheless proven difficult, owing to the multiplicity of eco- and replicable entity (12, 15, 60–62). logical and genetic factors interacting in the evolution of social Therefore, to show its utility in the explanation of the origin behavior, leaving for studies of sex-ratio conflicts the role of and evolution of eusociality, kin selection still needs to present prime tests of the theory (23–25, 27). Keller and Reeve (20), evidence for the existence of genes that work in the way that only summarizing a current consensus, conclude: ‘‘It is somewhat this theory predicts, that is to say, that spread because helping paradoxical that the outcome of within-colony conflicts provides relatives is genetically more productive than directly reproduc- one of the best demonstrations of kin-selection theory, a theory ing. It is true that those genes involved in within-colony conflicts that was first proposed to explain the evolution of extreme act by making individual carriers (e.g., workers) to promote the cooperation!’’ genes’ over-representation in the colony brood, but thus far, no In opposition to that view, here we questioned the suitability study has shown that such genes can act in a fecund individual of these studies for testing the role of kin selection on social in a way that affects its own reproduction. Genes that propagate evolution, and their increasingly frequent use for understanding by taking advantage of a social organization previously created, the social biology of eusocial organisms, coupled to a neglect of or genes that favor other copies without any reproductive cost, their phylogenetic and life history. Although elegantly demon- are not in this category. strating the emergence and outcome of conflicts between dis- tinct units of selection (genes and the eusocial colony in the We are grateful to John Tyler Bonner, Gabriel Dover, Alex Kacelnik, present case), they provide only limited evidence that the kind and the anonymous referees for helpful comments on the manuscript. of action attributed to kin-selected genes is the one that can lead Financial support was received from Coordenac¸˜ao de Aperfeic¸oamento to the development and evolution of individual or colonial de Pessoal de Nı´vel Superior, Brazil (CAPES).

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