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Sociobiology was founded by E.O. Wilson (1975) in a massive book of the same title. However what Wilson really did was to give a name to a field that was already being developed in evolutionary biology, the study of the adaptive value of social behavior. His contribution was important because he examined all aspects of social behavior then known with separate chapters on the behavior of birds, mammals, insects, and the like that were known in 1975 to live in groups and behave socially and whose behavior had been demonstrated to promote the reproductive or genetic success of individuals. The field would have probably remained uncontroversial were it not for the strong negative response of opponents led by some of Wilson’s own colleagues at Harvard, namely, Stephen Jay Gould and Richard Lewontin. These opponents, the self-named Science for the People, produced strongly worded attacks on the book Sociobiology and its author claiming that sociobiology incorporated outdated and incorrect approaches to social behavior (Allen et al. 1975, 1976). The vehemence of the opposition to an evolutionary analysis of social behavior was encapsulated in the desire with which the opponents sought to link Wilson with the Nazis, eugenics, and other discredited persons and activities despite the academic nature of his synthesis which barely touched upon human behavior, the focus of the opposition. This attack led to physical assaults on Wilson including the pouring of cold water on his head by a member of the Science for the People at a conference in which Wilson attempted to speak.
Among the objections raised by the opponents of sociobiology, who include Michael Rose (1998). He wrote that we rarely if ever wish to raise our genetic success when behaving socially. This is true enough but our proximate (immediate) desires get us to behave in ways that influence the transmission of our genes to subsequent generations. In other words, our wishes and emotions that cause us to behave in certain ways have evolutionary (long-term) significance. And proximate physiological systems therefore can evolve as certain proximate mechanisms lead to greater adaptive results, i.e., gene propagation, than others with the logical conclusion that those social desires that are associated with superior reproductive or genetic success will become more and more common over time in populations of social species.
Likewise, the objections that sociobiologists, like Wilson, are genetic determinists who believe in a one-to-one relationship between genes and behaviors, a point repeatedly raised by Stephen Jay Gould (1976, 1996), are misguided. The proximate genetic aspects of development of a person are not the essence of sociobiology which instead deals primarily with the possible adaptive functions of social behavior. Notice that the previous sentence states “possible adaptive functions” since the goal of sociobiology is to test hypotheses on the genetic value of possible adaptations associated with social behavior. As T.H. Huxley (1910), the great defender of Darwinian theory, wrote, “There is a wonderful truth in [the] saying [that] next to being right in this world, the best of all things is to be clearly and definitely wrong, because you will come out somewhere.”
This approach tells us that another chief criticism of sociobiology, particularly of humans, is without merit, namely, that evolutionary studies of social behavior contribute to social injustice and inequality which arise because of attempts to justify certain patterns of social behavior, a criticism raised by Science for the People (Allen et al. 1975, 1976). In reality, tests of hypotheses on the adaptive value of social behavior are designed to explain why we and other social organisms do what we do, not to justify that activity (Alcock 2001; Rubenstein and Alcock 2013), a point that is obvious when the social creature under examination is an insect rather than a human. No one argues that the stings of honey bees are justified by an analysis of the adaptive value of stinging by worker bees. The goal instead is to explain why workers sting and how this social behavior (colony members detect stinging by others and join the stingers) advances the success of the genes of the worker.
The Selfish Gene
Another extremely important book, The Selfish Gene, was written by Richard Dawkins (1976) about the same time as Sociobiology. In it Dawkins explained why the arguments of adaptationists (persons who rely on the theory of differential genetic success) were so useful for sociobiologists and behavioral ecologists, both of whom use Darwinian natural selection as the basis for their adaptationist hypotheses. Although Darwin was clueless about genetics, because Mendel’s work was unknown to him and other biologists prior to the early 1900s, his insights in On the Origin of Species (Darwin 1859) in which he presented the theory of natural selection provide the foundation for all modern evolutionary behavioral work, a point that Dawkins explained clearly – despite the arguments that others raised against the book, most of which deal with the title of the book. Dawkins spends the bulk of the introduction to the third edition in a defense of this title, The Selfish Gene, which some people insisted upon interpreting as meaning that Dawkins was saying that genes were selfish in a proximate sense rather than selfish in an evolutionary sense. As Dawkins notes, genes can cooperate proximately (developmentally) if the result of their cooperation is the promulgation of those genes against alternate forms that differ from the more successful genes. In his book, Dawkins showed how the fundamentally Darwinian evolutionary selfishness of genes was the product of natural selection with genes selected (becoming more common) on the basis of their copying success. He explained that since only genes survive from generation to generation, genetic success was more important than that of the individual or species or group in which the genes reside. Awareness of the gene encourages us to understand why genes can cooperate in the building of cooperative individuals whose help given to others results in additional copies of the genes in question. In the course of The Selfish Gene, Dawkins highlights the work of George C. Williams and William D. Hamilton, both of whom used the ideas of Charles Darwin to set the stage for the focus on the gene, showing how individual survival machines worked to pass on their genes to future generations, and thereby determined which genes would live on and which would die out as a result of Darwinian selection.
George C. Williams and the Essence of Sociobiology
G.C. Williams (1966) was the most important of these persons when it comes to sociobiology. His book, Adaptation and Natural Selection, made the case for individual selection (via the gene) as being far more significant than group- or species-level selection. He did so by contrasting the power of individual selection against that of group selection. He posed a thought question by asking his readers to consider what would happen if natural selection occurred and individuals sacrificed their reproductive success to benefit the group, an extremely widespread explanation for social behavior at the time, a point of view championed by V.C. Wynne-Edwards (1962). For example, territorial behavior was widely thought to evolve if non-territorial individuals promoted the survival of the species either because the non-territorial types were inferior or because breeding by these individuals would threaten the survival of the group through over-population. However, as Williams noted such a situation would be vulnerable to an invasion by genes that caused their owners to refuse to be non-territorial sacrificing themselves for the benefit of the group. If they passed on their genes to the next generation in time, there would be no non-territorial individuals possessing the genes for non-territoriality. In other words, if one observed both territorial and non-territorial members of a given species, one had to think of a way in which the non-territorial individuals experienced genetic success, not a way in which the group benefited from the behavior of the non-territorial types. The hypothesis that non-territorial individuals sacrificed for the territorial members was a non-starter.
In every situation in which group selection à la Wynne-Edwards was used to promote the idea that individuals gave up reproductive chances to help others of their species to reproduce, Williams’s explanation focused on the benefits to individuals to do what they did in order to secure genetic success. So, for example, if birds flew in large flocks to get information about the density of competitors in an area, the group selectionist explanation was that some birds used this information to reproduce less in order to help the species to avoid over-population. Williams proposed that some birds used this information to avoid trying to reproduce at times and places that would almost certainly have resulted in reproductive failure by the birds in question. This hypothesis had the virtue of not arguing that some birds would give up reproduction (and thus genetic success) to assist others, a recipe for the disappearance of those genes that induced some birds to sacrifice for others, whereas if by giving up reproduction temporarily, those individuals had more surviving offspring in their lifetime than they would otherwise, the genes for using density information to regulate reproduction could spread through a population.
Male Lion Social Behavior: Coalitions of Unrelated Individuals
Male lions often form groups that seek to take prides of females from other males, a social behavior that can be understood as way in which individual lions seek to pass on their genes. Although these groups are sometimes composed of relatives, a fact that makes groups of this sort understandable in a Hamiltonian sense (see below), sometimes the groups are made up of unrelated males. The question is how does one account for groups of non-relatives in Williams’s terms? As it turns out, cooperation of the sort seen in lions can evolve by natural selection if it generates increased reproductive success for the cooperators even if some males reproduce less than others. Thus, if several unrelated males succeed in securing a pride, their reproductive success merely has to be greater than it would otherwise in order to support a hypothesis that explains their social behavior in terms of individual genetic success as opposed to group benefit selection. (Again there are logical reasons in favor of the individual selection hypothesis that makes this explanation worth considering, whereas the group selection alternative is untenable if the hypothesis requires that unrelated individuals sacrifice their reproduction to benefit the group or species.) All the unrelated males stand to pass on some of their genes if through their cooperativeness they defeat another group of males, ousting them from a pride of adult females. Thus the individual selection hypothesis not only does not require that some male lions sacrifice their reproductive chances to help other males in the coalition, this explanation also generates predictions that can be checked, thereby testing the individual selection hypothesis. We can predict that when non-relatives join together, they will do so to take a pride from a smaller coalition of males. Moreover, those non-relatives that have no or little genetic success (i.e., if other males do most or all of the mating) and then those unrelated males that cooperate in securing a pride but have little reproductive success should weigh less than the dominant lions in the group. Males that weigh less than average are expected to be handicapped in the effort to secure a pride that will generally be held by groups of males favoring those that join others in defeating groups of rivals that control a pride. The point here is that the opportunity for some reproductive success (i.e., genetic success) is better than none. Single males that fail to secure a pride when up against groups are expected to have no reproductive success at all.
Male Lion Social Behavior: Coalitions of Related Individuals
Male lions often form groups composed of relatives, and in this case there is yet another hypothesis that looks to the genes of the males in the coalition for an explanation for their social behavior. Relatives (brothers, half-brothers, and cousins) share genes in common as a result of having a shared ancestor. The reason why W.D. Hamilton (1964) is viewed as an admired and influential theorist in sociobiology has to do with his focus on shared genes that led him to point out that although reproduction enables an individual to transmit genes directly to the next generation, helping relatives reproduce can achieve the same end indirectly. Therefore if a coalition of male lions is composed of relatives, even those individuals that have little or no genetic success via reproduction can pass on their genes indirectly – if they help their relatives reproduce successfully. Therefore one can predict that in coalitions of related males, reproduction by some individuals will be helped by the non-reproductive lions (primarily in the takeover of prides from other groups of males). In other words, some indirect genetic success is better than none, and no genetic success would be the typical fate of those solitary individuals that did not help related males to acquire prides of females.
After Hamilton’s argument was published, it has become extremely important in accounting for many cases of social behavior in which the key prediction is that groups of cooperators will be composed of relatives (primarily close relatives with a high proportion of shared genes).
Acceptance of Genic vs Group Benefit Selection
It is safe to say that the vast majority of sociobiologists and behavioral ecologists have accepted the views of Williams and Hamilton and rarely if ever bother to test illogical group selectionist hypotheses about the benefits of social behavior to groups or species as a whole. There are however several researchers who continue to try to argue that group selection is important to the evolutionary process rather than direct gene (personal reproduction) or indirect gene (help given relatives) selection. Among these theorists is E.O. Wilson who has abandoned his view that the vast majority of cases of social behavior can be explained in terms of direct or indirect gene transmission in favor of the position that group selection accounts for much of the social behavior of organisms. He appears to have been persuaded by David Sloan Wilson (not a relative of E.O. Wilson), a long-time advocate for group-level selection, to change his support for sociobiology in 2007 (Wilson and Wilson 2007).
However, none of these advocates for group selection has had much success in converting others to their viewpoint. For most sociobiologists the social behavior of individuals is to be investigated using the principles of Williams or Hamilton. This point can be made by showing how research on the adaptive value of animal social behavior has either examined the reproductive importance of the behavior to social individuals (with each individual produced by personal reproduction carrying half the genes of the reproducer) or how individuals help their relatives reproduce (and thereby secure genetic success in proportion to the relatedness of the individual that they help) as illustrated by male lion social behavior.
So, for example, both males and females form social units in many species. These were once interpreted as primarily cooperative, and of course there is much that is cooperative about male-female bonds. However, the aspect of pairing that reflects Williams’s approach most clearly is research into conflicts between males and females, research by sociobiologists and behavioral ecologists (many sociobiologists prefer to be called behavioral ecologists thanks to the unhappy start of the field of sociobiology) that has exploded in the years since the publication of Williams’s book. These conflicts can and do occur as individuals of both sexes try to leave the offspring in the care of the other member of the pair. Males are especially likely to abandon their progeny in many species in order to inseminate as many females as possible since male reproductive success is often a function of the number of mates a male has whereas female reproductive success is more often linked to the quality of the mate, rather than the number of sexual partners acquired. The rarity of monogamy by males speaks to this argument and to the value of Williams’s position.
More Cases of the Utility of Individual Selection, Including More Examples of Sexual Conflict
In fact the resistance to mating exhibited by females of many species reduces the reproductive success of the rejected males and as such constitutes sexual conflict that arises because females are not equally receptive to all males in most cases. In addition, in species in which females eat males that approach them, we have further evidence of sexual conflict because it is rarely advantageous for a male animal to be consumed by a potential partner.
In insects females commonly exhibit an immune response that enables the females to avoid sexually transmitted diseases but that reduces the reproductive success of males if it kills some of their sperm. Evidence that such a response occurs in a cricket has been assembled by Fedorka and Zuk (2005) along with the finding that males attempt to suppress the immune response of females, further evidence that sexual conflicts are widespread in insects.
Williams’s argument also receives support from studies of many other elements of social behavior such as parental care of parasites by birds. Although some birds take care of parasitic species, an apparently maladaptive behavior, when work is done on the genetic benefits and genetic costs of doing so, one usually finds that the costs outweigh the benefits of ceasing to feed the parasitic offspring or abandoning the nest. These costs to reproductive success include the risk that a parasitic bird(s) might return to the nest of its host to destroy the eggs in the nest of the host (Soler et al. 1995).
Acceptance of Indirect Selection
Although Williams caused most sociobiologists and behavioral ecologists to examine hypotheses on the reproductive value of social behaviors, often it is clear that the behavior is altruistic, that is, the behavior helps others at the cost of reducing the reproductive output of the helper. Under these conditions, an alternative solution to this puzzle is required that does not involve group benefits of some sort. Here Hamilton’s approach has been often used by showing the altruist is related to the individual he or she helps, thereby increasing the representation of the altruist’s genes in the next generation. As documented already, this approach makes sense of the behavior of male lions, some of which form coalitions of relatives that are large enough to overcome the coalitions of other males that monopolize the sexual output of the pride of lionesses that they control. In order to use this approach however, one has to show that the loss of reproduction by the altruistic helper is exceeded by the gain in its genetic success as measured by the genes passed on as a result of the help. So, for example, an altruist that helps a brother produce two more offspring than he would otherwise have gains two times a half or 1 genetic unit since brothers are related by a half to the altruist and to their own offspring. If the cost of its helpful behavior is the loss of two offspring produced personally by the altruist, then the loss is two times a half or 1 genetic unit as well. In other words, in this case both altruism and personal reproduction are equally effective in passing on the genes of both types of behavior, indirectly and directly.
Cases Demonstrating the Utility of Indirect Selection
Hamilton’s approach has been widely adopted for lions and certain other mammals, those birds that nest in groups in which some individuals appear to help others reproduce, and social insects where altruism by workers is widespread. A mammal in which helping by relatives has evolved is the naked mole-rat (Sherman et al. 1991). This odd hairless mammal lives in underground colonies in Africa with large numbers of altruistic worker mole-rats that help a single reproducing “queen” and a small number of males that sometimes pass on their genes by mating with the female in charge of the colony. The helpful altruists that dig tunnels through the soil and secure tuberous food for the queen and kings are all progeny of the reproductive members of the colony as expected by Hamiltonian researchers.
In any event, the prediction that follows from the Hamiltonian approach is that helpers that are related to the parents that they help must increase the number of siblings that are generated in the nest. This outcome is generally observed in cases in which the prediction has been examined. Thus in the yellow-fronted miner (an Australian honeyeater), it has been shown that nests with helpers are more productive than nests without helpers. The same applies to the noisy miner with the further findings that males are more likely to help than females (which are able to reproduce sooner than males) and the effort expended by related individuals is greater than that engaged in by non-relatives (Barati et al. 2018). In bell miners, males are also more likely to help than females, and furthermore, helper males are typically fathered by parent males that mate with a single female so that helpers are more closely related to the siblings they provision and protect than they would be if their fathers mated with several females (which would mean that the relatedness of offspring was diluted by the different genes present in the eggs of those females). These results support predictions that a Hamiltonian would make and thus provide support for the hypothesis that relatedness is the cause of much helping at the nest in birds. In the long-tailed tits of Europe, altruistic helpers focus on nestling relatives over 90% of the time showing the kind of preference that has been predicted by indirect selection proponents.
Insect Sociality and Altruism
Thus in vertebrate mammals and birds, Hamilton’s ideas can supply a solution for the puzzle caused by help given to some individuals by others. However, most of the altruistic mammals and birds go on to reproduce. Although in some insects helpers have the capacity to reproduce, in others some individuals spend their entire lives working for others and indeed have rudimentary reproductive organs so that they could not reproduce even if they tried to do so. Among the insects, altruists are especially well represented in the bees, wasps, and ants.
Eventually the nest is used to produce a group of reproductively active males that seek out adult females and inseminate them; these females spend the winter in a safe place, and if all goes well, they become the foundress females at nests that contain a new generation the following year, an annual cycle that is covered by Evans and Eberhard (1970). If a worker female lays an egg in one of the brood cells of the nest, the reproductive female or a fellow worker will generally consume that egg, preventing the worker from reproducing, which it can do but is usually unable to do because of removal of its eggs from the nest. Indeed, the greater the genetic difference between a queen’s sons and the sons of workers, the more likely the eggs of workers are to be destroyed by fellow nestmates in the wasps, bees, and ants. In other words, when worker offspring are less closely related to other workers than to the offspring of the reproductive individuals, the more likely their eggs are to be eaten by other workers and queens (Wenseleers and Ratnieks 2006).
More importantly, worker paper wasps are all female, instead of mostly male as they are in honeyeaters and other birds. One assumes that the prevalence of female workers in wasps, ants, and bees stems from the ability of females in these groups to sting, which can deter predators from assaulting the nest with its edible larvae.
By far the most well studied of Hymenoptera are the honey bees, Apis mellifera, whose queens lay thousands of eggs destined to become daughter workers that help the queen manage the colony, feed the brood, and sacrifice themselves in stinging vertebrates that would plunder the hives if not checked. (The worker bees commit suicide when stinging animals with flexible skin in which their stingers catch, pulling out the still functional stinger and the internal organs of the worker). Since honey bees are the offspring of the queen and are related to any future queens, they can engage in helping behavior if their actions benefit the queen or a future queen (Seeley 1995). Half of the hive (largely female workers) will stay with a reproductive daughter of the queen when the queen leaves in a swarm to find a new nest. These workers clearly benefit the future queen, a sister of theirs, and so altruism can spread through the colony. The reduced ovaries of the worker females mean that they have little chance to reproduce personally so that there altruism can be adaptive.
Haplo-diploid Sex Determination and Indirect Selection
William Hamilton also thought that the method of sex determination of ants, bees, and wasps (all of which are placed in the order Hymenoptera) could have something to do with the evolution of helping by relatives in these groups. In the Hymenoptera, including the honey bee, males are haploid (have only one set of chromosomes donated by the mother), and females are diploid (with two sets derived from both parents) unlike most vertebrates in which both sexes are diploid and differences in sex chromosomes are the basis for sexual differences between males and females (although in some species of turtles and crocodilians egg temperature determines the sex of the individual). Nevertheless female hymenopterans are unusual in being able to lay unfertilized eggs that develop into haploid males, whereas only fertilized female queens can produce diploid daughters.
Hamilton noted that the daughters of female queen hymenopterans that had mated with only one male would all receive that male’s haploid set of chromosomes plus half of the mother’s diploid makeup. The half received from the mother could be the same for two daughters or completely different for these two daughters or somewhere in between the same and totally different. As a result, the average similarity between two daughters would be ½ (from the father if the mother hymenopteran mated with a single male) + ¼ (the average from the mother’s genes) or 3/4, a figure that is higher than that for diploid-diploid organisms where on average two offspring, whether daughters or sons, would have inherited half their genes in common from both parents. (See Rubenstein and Alcock for additional information on the significance of haplo-diploid sex determination.) If daughter workers possess 3/4 of the genes that reproductive females have, then helping future queens could be very adaptive (genetically speaking) for sterile or male-producing wasps, bees, or ants. The same logic says that worker hymenopterans should make three times as many would-be queens as would-be kings, a prediction that has been found to be generally correct. Hamilton noted that in many Hymenoptera females do mate with just one male and that in these species female workers do tend to help reproductively competent sisters, as predicted, which supports the sex determination hypothesis for female altruism in this group of insects.
Other Examples of the Utility of Indirect Selection as Explanations for Altruism
Research on bacteria has shown that individuals can recognize one another and behave positively toward those that are similar genetically unless there is competition for limited resources. Because bacteria often form colonies or clones of genetically identical individuals, altruism that costs the donor bacteria can spread if it benefits the recipients (provided that the recipients are closely related to the altruists as they would be in a clone). The release of a substance from the altruists that helps the receiver bacteria is the sort of behavior that could evolve by indirect selection. In fact, cooperation occurs not only among bacteria but also in a host of other situations including cooperation among organelles within an individual and the cooperation exhibited by different cells in the building of an individual. In many cases in which the organelles and cells are in the same body and have the same genes, the cooperation that exists between them represents indirect selection at work (West et al. 2007).
However, not all cases of altruism have a straightforward explanation. Thus, when starving slime molds cells come together in order to produce a stalk on which reproductive spores are situated, cooperation occurs in the growth of a stalk that does not participate in the production of spores, although the height of the stalk can influence the dispersal of the spores. When all this happens with genetically identical cells, the growth of a stalk can be explained as the result of altruism by cells that are genetically identical to the cells that will form the reproductive units of the slime mold. But when you artificially mix two clones, as sometimes occurs in nature, the two clones often contribute cells unequally to the non-reproductive stalk so that if 50% of the mixture is of clone A, the stalk may be made up of less than 50% of clone A cells. In cases in which the stalk is largely composed of clone B cells, this suggests that clone A is exploiting clone B for its reproductive purposes (Strassmann et al. 2000). Thus the social behavior of clones of slime molds indicates that both direct and indirect selection are probably at work in determining the outcome of the stalk construction and the development of the spores, but the issue has yet to be fully resolved. When the issue of stalk formation is completely solved, Williams’s and Hamilton’s principles of genic selection will almost certainly be used by researchers studying the social behavior of slime molds.
Despite the controversies associated with the early stages of sociobiology, the field has been producing ever more studies over the last 45 years, and it seems certain that it will flourish in the future. The work of G.C. Williams in showing that Darwinian theory is best used to develop and test hypotheses on how the social behavior of individuals enhances the reproductive success of individuals, and not the survival of social groups or species, has been critical in establishing the utility of sociobiology. In addition, the insights of W.D. Hamilton in demonstrating that individuals can propagate their genes indirectly, especially by helping relatives reproduce, have shown that genic selection is the key to understanding the evolution of social behavior of individuals whether mammals, birds, insects, or even bacteria. Together the two approaches have provided sociobiological researchers with two essential tools to explain why in evolutionary terms organisms have hit upon social life as a means to pass on their genes to future generations and so influence the evolution of social behavior.
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