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Haplodiploidy and evolution of social insects

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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.
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... However, haplodiploidy also results in females being less related to their brothers (r = 0.25) than to their sons, exactly cancelling out the benefit of super-sister relatedness [20,21]. Sex ratios that are split either temporally (i.e., across broods) or demographically (i.e., female-biased ratios in potential altruists' nests and male-biased in solitary nests) are therefore required for helpers to take advantage of sister super-relatedness [6,22,23]. ...
... Second, a proportion of first brood males must survive long enough to compete with second brood males for matings with second brood females. This increases the reproductive value of males relative to females in the first brood, because by mating with females of both broods, first brood males produce more offspring than do first brood females [6]. This, in turn, leads foundresses to produce a male-biased first brood sex ratio. ...
... Eusociality is a complex social system characterised by division of labour between reproductive (queens) and non-reproductive (worker) castes, the latter of which forfeit their own reproduction to help raise genetic relatives, typically siblings [1,2]. Why a daughter would help raise the offspring of her mother at the cost of her own reproduction has been investigated by some of the most influential evolutionary biologists [3][4][5][6][7]. For helping behaviour to evolve, conditions must be present that make the indirect fitness benefits of helping outweigh the cost of foregoing personal reproduction that is paid by the helper [6,8]. ...
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Eusociality, where workers typically forfeit their own reproduction to assist their mothers in raising siblings, is a fundamental paradox in evolutionary biology. By sacrificing personal reproduction, helpers pay a significant cost, which must be outweighed by indirect fitness benefits of helping to raise siblings. In 1983, Jon Seger developed a model showing how in the haplodiploid Hymenoptera (ants, wasps and bees), a partially bivoltine life cycle with alternating sex ratios may have promoted the evolution of eusociality. Seger predicted that eusociality would be more likely to evolve in hymenopterans where a foundress produces a male-biased first brood sex ratio and a female-biased second brood. This allows first brood females to capitalize on super-sister relatedness through helping to produce the female-biased second brood. In Seger’s model, the key factor driving alternating sex ratios was that first brood males survive to mate with females of both the second and the first brood, reducing the reproductive value of second brood males. Despite being potentially critical in the evolution of eusociality, however, male survivorship has received little empirical attention. Here, we tested whether first brood males survive across broods in the facultatively eusocial sweat bee Halictus rubicundus . We obtained high estimates of survival and, while recapture rates were low, at least 10% of first brood males survived until the second brood. We provide empirical evidence supporting Seger’s model. Further work, measuring brood sex ratios and comparing abilities of first and second brood males to compete for fertilizations, is required to fully parameterize the model.
... Therefore, the perusal of sex ratio evolution in these insects is one of the important aspects of studying their sex allocation (Charnov 1982) and the effect of kin selection on social behavior (Trivers 1985). Trivers and Hare (1976) looked into the sex ratio theory of Fisher's (1930) and kin selection theory of Hamilton (1964) and then, regarding hymenopterans opined that the stable ratio from the queen's viewpoint is 1:1, because queens are equally related to daughters and sons. However, the stable ratio from the worker's viewpoint is 3:1, i.e., female to male ratio. ...
... This is because haplodiploidy (i.e., the production of males from haploid eggs) causes workers to be three times more closely related to sisters than to their brothers. Trivers and Hare (1976) therefore, deduced that workers should usually control sex allocation because they typically outnumber queens and rear the brood. In many species of Hymenoptera, that depict social behavior, there is a female-biased sex ratio (Bourke andFranks 1995, Crozier andPamilo 1996). ...
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... The remaining fraction of the new queens is produced by sexual reproduction. Queens also reproduce through arrhenotokous parthenogenesis (originating males by asexual reproduction) to produce new haploid males, as it is classically the case in Hymenoptera (Trivers and Hare 1976). This unusual reproductive system reduces male gene flow and limits genetic mixing in reproductive individuals, as most of the new queens and all males are asexually produced. ...
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Low dispersal, occurrence of asexual reproduction and geographic discontinuity increase genetic differentiation between populations, which ultimately can lead to speciation. In this work, we used a multidisciplinary framework to characterize the genetic and phenotypic differentiation between and within two cryptic ant species with restricted dispersal, Cataglyphis cursor and C. piliscapa and used behavioral experiments to test for reproductive isolation. Their distribution is segregated by the Rhône River and they have been traditionally distinguished only by hair numbers, although a statistical assessment is still lacking. We found strong genetic (microsatellites, nuclear and mitochondrial sequences), morphological (number of hairs, tibia length, male genitalia) and chemical (cuticular hydrocarbons) differentiation not only between species but also among localities within species. However, inter-specific differentiation was slightly higher than intra-specific differentiation for most markers. Overall, this pattern could either reflect reproductive isolation or could result from a longer period of geographic isolation between species than among localities within species without necessarily involving reproductive isolation. Interestingly, our behavioral experiments showed an absence of mating between species associated to a higher aggressiveness of workers towards heterospecific males. This suggests that sexual selection may, at least partially, fuel reproductive isolation. We also showed that cuticular hydrocarbons, mtDNA sequences and number of hairs provide reliable criteria allowing species discrimination. Overall, this species complex offers a case study to further investigate varying stages of a speciation continuum by estimating reproductive isolation between pairs of localities varying by their level of genetic differentiation.
... According to the former models, sex is advantageous regardless of reciprocal gene exchange, while the latter models assume that sex allows reciprocal gene exchange (crossing over) promoting genetic diversity and response to selection among the progeny. Briefly, immediate benefit hypotheses have proposed that sex is advantageous as (1) it increases the fitness of progeny (Dougherty 1955;Lloyd 1980;Bernstein and Bernstein 1991), (2) reduces the deleterious mutation rate (Bengtsson 1986;Ettinger 1986;Holliday 1988), or 3) increases the efficiency of selection (Geodakyan 1965;Trivers and Hare 1976). Variation and selection hypotheses include the (1) environmental stochastic (Morgan 1913;Fisher 1930;Muller 1932;Manning and Jenkins 1980;Manning 1982), (2) environmental deterministic (Sturtevant and Mather 1938;Mather 1943;Eshel and Feldman 1970;Treisman 1976;Charlesworth 1976), (3) mutational stochastic (Muller 1964), (4) drift (e.g., by generating negative linkage disequilibrium- Otto and Lenormand 2002), and (5) mutational deterministic models (Kondrashov 1982;Crow and Simmons 1983). ...
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Understanding why sexual reproduction—which involves syngamy (union of gametes) and meiosis—emerged and how it has subsisted for millions of years remains a fundamental problem in biology. Considered as the essence of sex, meiotic recombination is initiated by a DNA double-strand break (DSB) that forms on one of the pairing homologous chromosomes. This DNA lesion is subsequently repaired by gene conversion, the non-reciprocal transfer of genetic information from the intact homolog. A major issue is which of the pairing homologs undergoes DSB formation. Accumulating evidence shows that chromosomal sites where the pairing homologs locally differ in size, i.e., are heterozygous for an insertion or deletion, often display disparity in gene conversion. Biased conversion tends to duplicate insertions and lose deletions. This suggests that DSB is preferentially formed on the “shorter” homologous region, which thereby acts as the recipient for DNA transfer. Thus, sex primarily functions as a genome (re)loading mechanism. It ensures the restoration of formerly lost DNA sequences (deletions) and allows the efficient copying and, mainly in eukaryotes, subsequent spreading of newly emerged sequences (insertions) arising initially in an individual genome, even if they confer no advantage to the host. In this way, sex simultaneously repairs deletions and increases genetic variability underlying adaptation. The model explains a remarkable increase in DNA content during the evolution of eukaryotic genomes.
... A key inspiration that, in his mind, helped transform his vast catalog of individual species behaviors into the "common principles" he had been seeking was Hamilton's 1964 article on kin selection, which he read with astonishment and quickly handed to me during my first graduate year, both to confirm and to firm up his grasp of the mathematical treatment, and he expressed the view that if the article was correct, it revolutionized our understanding of the evolution and nature of the social behavior of at least the Hymenoptera and quite possibly that of many other species as well. In Sociobiology, he continued to be excited by kin selection, as modified by consideration of sex ratio (Trivers and Hare 1976), asserting that "nothing but kin selection seems to explain the statistical dominance of eusociality by the Hymenoptera" (pp. 417-418) and invoking it for certain other species as well (e.g., several jay species). ...
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