Coefficients of Relationship and the Identity of Genes by Descent in the Hymenoptera
TL;DR: Although Hamilton 's calculations are in error for some relationships involving males, the coefficients of relationship given by Wright (1922; see Li 1955) are also inadequate for determining the optimum strategy of an individual based on the probable degree of relatedness of another to it.
Abstract: Hamilton (1964a) has pointed out that social behavior can evolve through kinship selection, wherein the probability of an altruistic act is proportional to the probable genetic relationship between altruist and recipient. Therefore, to calculate likelihoods of altruistic behavior being evolved in certain situations, the probable proportions of genes identical by descent in the individuals involved must be known. Haplodiploidy, the basic genetic system in Hymenoptera, is particularly favorable for the evolution of altruistic behavior, since full sisters have three-fourths of their genes identical by descent (Hamilton 1964b). This is because they each receive the same haploid set of chromosomes from their father, making up half their genotypes, while genes from their mother, being the products of a normal meiosis, are identical by descent half of the time. Full sisters under normal autosomal inheritance, where both sexes are diploid, have only half their genes identical by descent. When I compared a number of other coefficients of relationship calculated by Hamilton (1964b) with those given by Li (1955), however, I observed several discrepancies. In some cases it was also clear that Hamilton's values must be in error. For example, since brothers, being haploid and impaternate, are the equivalents of gametes produced by the meiosis of one individual, they clearly have half their genes in common; yet Hamilton (1964b) gives a coefficient of relationship of r 1/4 for this relationship. This erroneous result is due to Hamilton 's treatment of males in calculating coefficients of relationship: each male is artificially \"made diploid\" by the addition of a \"cipher \" gene that is unique to it. Although Hamilton 's calculations are in error for some relationships involving males, the coefficients of relationship given by Wright (1922; see Li 1955) are also inadequate for determining the optimum strategy of an individual based on the probable degree of relatedness of another to it. This is because the coefficient of relationship as usually employed is actually a measure of phenotypic correlation assuming simple additive gene effects, rather than an estimate of the proportion of genes held in common through identical descent, although in normal autosomal inheritance the values obtained are correct for either purpose. Another failing of the coefficient of relationship is that it makes no distinction between the relationship of a given male to a given female and the converse female-male relationship. Thus the value r = 1/2 is obtained for the father-daughter relationship (Li 1955), whereas in fact all the father's genes are identical by descent with genes present in the daughter, while only half the daughter's genes are identical by descent with genes present in the father. The situation is, however, clearly indicated by Lji's diagrams (1955, p. 182). Letting GA(B) be the proportion of individual A's
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TL;DR: Evidence is presented from 20 species that the ratio of investment in monogynous ants is, indeed, about 1 : 3, and this discovery is subject to a series of tests, which provide quantitative evidence in support of kinship theory, sex ratio theory, and the assumption that the offspring is capable of acting counter to its parents' best interests.
Abstract: Halminton (1) was apparently the first to appreciate that the synthesis of Mendelian genetics with Darwin's theory of natural selection had profound implications for social theory. In particular, insofar as almost all social behavior is either selfish or altruistic (or has such effects), genetical reasoning suggests that an individual's social behavior should be adjusted to his or her degree of relatedness, r, to all individuals affected by the behavior. We call this theory kinship theory. The social insects provide a critical test of Hamilton's kinship theory. When such theory is combined with the sex ratio theory of Fisher (9), a body of consistent predictions emerges regarding the haplodiploid Hymenoptera. The evolution of female workers helping their mother reproduce is more likely in the Hymenoptera than in diploid groups, provided that such workers lay some of the male-producing eggs or bias the ratio of investment toward reproductive females. Once eusocial colonies appear, certain biases by sex in these colonies are expected to evolve. In general, but especially in eusocial ants, the ratio of investment should be biased in favor of females, and in it is expected to equilibrate at 1 : 3 (male to female). We present evidence from 20 species that the ratio of investment in monogynous ants is, indeed, about 1 : 3, and we subject this discovery to a series of tests. As expected, the slave-making ants produce a ratio of investment of 1 : 1, polygynoys ants produce many more males than expected on the basis of relative dry weight alone, solitary bees and wasps produce a ratio of investment near 1 : 1 (and no greater than 1 : 2), and the social bumblebees produce ratios of investment between 1 : 1 and 1 : 3. In addition, sex ratios in monogynous ants and in trapnested wasps are, as predicted by Fisher, inversely related to the relative cost in these species of producing a male instead of a female. Taken together, these data provide quantitative evidence in support of kinship theory, sex ratio theory, the assumption that the offspring is capable of acting counter to its parents' best interests, and the supposition that haplodiploidy has played a unique role in the evolution of the social insects. Finally, we outline a theory for the evolution of worker-queen conflict, a theory which explains the queen's advantage in competition over male-producing workers and the workers' advantage regarding the ratio of investment. The theory uses the asymmetries of haplodiploidy to explain how the evolved outcome of parent-offspring conflict in the social Hymenoptera is expected to be a function of certain social and life history parameters.
1,183 citations
TL;DR: With better knowledge of heredity and with more facts regarding the social insects to draw upon, Weismann recognized the possible conflict between intergroup and intragroup selection in the evolution of worker attributes.
Abstract: In what sense can the self-sacrificing sterile ant be considered to "struggle for existence" or to endeavor to maximize the numbers of its descendants? Since the founding of the theory of evolution by natural selection, most biologists have evaded this question by focusing attention exclusively on the colony as the reproducing unit. There is a powerful precedent for this. Darwin himself took this course. He saw only a "minor" difficulty in the evolution of sterility, and he passed over it in a few lines as he proceeded to discuss the "great" difficulty of how the special aptitudes of the workers could be passed on in latent form by their fertile sisters (26). A difficulty over sterility exists, nevertheless, and it is the more surprising that Darwin should have passed over it in that he discussed-but left unsolved-a parallel one raised by the social virtues (courage and self-sacrifice) in man (25). He saw that such qualities would be promoted in intergroup selection but counter-selected within each group. Perhaps the possible avenues of indiscipline in social insects had been so little reported in Darwin's time that the problems they raised were easily overlooked. Darwin's inadequate understanding of heredity may, likewise, have helped to keep the problem out of focus. With better knowledge of heredity and with more facts regarding the social insects to draw upon, Weismann (154) recognized the possible conflict between intergroup and intragroup selection in the evolution of worker attributes. He made the perceptive comment that, "Obviously the workers must be more rapidly improved when all in a hive are progeny of one queen-i.e. they are all alike or almost alike." But this comment was made in the course of discussion of another topic, and he did not pursue the matter. Soon Mendelian genetics resolved Darwin's difficulty of latency, apart from details of mechanism. But the disappearance of this problem does not seem to have given greater prominence to the other, and the question of how worker sterility comes to be selected continued to receive only occasional comment for a long time. Sturtevant (142) in 1938 again outlined it with admirable clarity and with special reference to multiqueened (polygynic) organization, which was by then well known. Rau (118) in 1940 also briefly touched on this crux when he noted how small might be the step separating workerlike behavior in auxiliary Polistes queens 193
1,146 citations
TL;DR: It is shown that unbiased estimates of relatedness cannot be obtained at the individual level without knowledge of the allelic distributions in both the individuals of interest and the base population unless the proportion of shared marker alleles between unrelated individuals is essentially zero.
Abstract: The recent discovery of hypervariable VNTR (variable number of tandem repeat) loci has led to much excitement among population biologists regarding the feasibility of deriving individual estimates of relatedness in field populations by DNA fingerprinting. It is shown that unbiased estimates of relatedness cannot be obtained at the individual level without knowledge of the allelic distributions in both the individuals of interest and the base population unless the proportion of shared marker alleles between unrelated individuals is essentially zero. Since the latter is usually on the order of 0.1-0.5 and since there are enormous practical difficulties in obtaining the former, only an approximate estimator for the relatedness can be given. The bias of this estimator is individual specific and inversely related to the number of marker loci and frequencies of marker alleles. Substantial sampling variance in estimates of relatedness arises from variation in identity by descent within and between loci and, with finite numbers of alleles, from variation in identity in state between genes that are not identical by descent. In the extreme case of 25 assayed loci, each with an effectively infinite number of alleles, the standard error of a relatedness estimate is no less than 14%, 20%, 35%, and 53% of the expectation for full sibs and second-, third-, and fourth-order relationships, respectively. Attempts to ascertain relatedness by means of DNA fingerprinting should proceed with caution.
437 citations
TL;DR: It is the view that a whole series of factors acting jointly or alternately is responsible for the numerous origins of sociality in Hymenoptera, compared to only one in all the other insects.
Abstract: Kin selection has been used to explain evolution of man altruistic traits found in those social insect castes which have reduced reproductivity. Kin selection is most probable among organisms living in family groups. It is commonly assumed, therefore, that (1) the most primitive social insects, like the more specialized ones, live in mother-daughter (eusocial) colonies, (2) colonies of individuals of the same generation and showing castes (semisocial colonies) are abnormal or originate only in inbreeding populations, and (3) transfer of individuals among colonies must be selected against, except in inbreeding populations. Numerous Hymenoptera are cited, however, in which semisociality or transfer occurs in populations lacking evidence for inbreeding; and we believe that, in explaining the origin of social behavior in insects, Hamilton and others have placed too much emphasis on the evolution of altrustic behavior through kin selection. There is considerable evidence that social behavior in insects is in p...
403 citations
TL;DR: It is shown that the genetic structure of the A. mellifera colony remained largely unchanged over time as long as the colony is headed by the same queen, and the genetic diversity within the colony provided a good estimate of the genetic Diversity of the local honeybee population.
Abstract: Sociobiologists have long sought to estimate precisely the relatedness among members of social insect colonies because of the central significance of kinship in evolutionary and behavioural studies. By using microsatellites, we directly identified the 7-20 subfamilies (patrilines) present in five honeybee colonies belonging to three different subspecies ( Apis mellifera mellifera, A. m. carnica and A. m. ligustica ). By focusing further investigations on one A. m. mellifera colony, we showed that the genetic structure remained largely unchanged over time as long as the colony is headed by the same queen. The genetic diversity within the colony also provided a good estimate of the genetic diversity of the local honeybee population. The distribution of patrilines was significantly different in swarming workers compared with contemporaneous pupae of the original colony, probably due to unequal propensities for swarming among patrilines. Conversely, no bias in the relative proportions between worker and queen brood could be detected.
352 citations
Additional excerpts
...Among the different coefficients available to measure relatedness between individuals, the pedigree coefficient of relatedness (G), introduced by Crozier (1970), was chosen because of its significance and interest in the study of the evolution of social behaviour (Pamilo & Crozier 1982)....
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TL;DR: A genetical mathematical model is described which allows for interactions between relatives on one another's fitness and a quantity is found which incorporates the maximizing property of Darwinian fitness, named “inclusive fitness”.
14,730 citations
TL;DR: The importance of having a coefficient by means of which the degree of inbreeding may be expressed has been brought out by Pearl' in a number of papers published between 1913 and 1917.
Abstract: IN the breeding of domestic animals consanguineous matings are frequently made. Occasionally matings are made between very close relatives-sire and daughter, brother and sister, etc.-but as a. rule such close inbreeding is avoided and there is instead an attempt to concentrate the blood of some noteworthy individual by what is known as line breeding. No regular system of mating such as might be followed with laboratory animals is practicable as a rule. The importance of having a coefficient by means of which the degree of inbreeding may be expressed has been brought out by Pearl' in a number of papers published between 1913 and 1917. His coefficient is based on the smaller number of ancestors in each generation back of an inbred individual, as compared with the maximum possible number. A separate coefficient is obtained for each generation by the formula
1,928 citations