Consequences of population structure for sex allocation and sexual conflict.

Both sex allocation and sexual conflict can be modulated by spatial structure. However, how the interplay between the type of dispersal and the scale of competition simultaneously affects these traits in sub-divided populations is rarely considered. We investigated sex allocation and sexual conflict evolution in meta-populations of the spider mite Tetranychus urticae evolving under budding (pairing females from the same patch) or random (pairing females from different patches) dispersal and either local (fixed sampling from each subpopulation) or global (sampling as a function of subpopulation productivity) competition. Females evolving under budding dispersal produced less female-biased offspring sex ratios than those from the random dispersal selection regimes, contradicting theoretical predictions. In contrast, the scale of competition did not strongly affect sex allocation. Offspring sex ratio and female fecundity were unaffected by the number of mates, but female fecundity was highest when their mates evolved under budding dispersal, suggesting these males inflict less harm than those evolving under random dispersal. This work highlights that population structure can impact the evolution of sex allocation and sexual conflict. Moreover, selection on either trait may reciprocally affect the evolution of the other, for example via effects on fecundity.

Competition and fixation of cohorts of adaptive mutations under Fisher geometrical model.

One of the simplest models of adaptation to a new environment is Fisher's Geometric Model (FGM), in which populations move on a multidimensional landscape defined by the traits under selection. The predictions of this model have been found to be consistent with current observations of patterns of fitness increase in experimentally evolved populations. Recent studies investigated the dynamics of allele frequency change along adaptation of microbes to simple laboratory conditions and unveiled a dramatic pattern of competition between cohorts of mutations, i.e., multiple mutations simultaneously segregating and ultimately reaching fixation. Here, using simulations, we study the dynamics of phenotypic and genetic change as asexual populations under clonal interference climb a Fisherian landscape, and ask about the conditions under which FGM can display the simultaneous increase and fixation of multiple mutations-mutation cohorts-along the adaptive walk. We find that FGM under clonal interference, and with varying levels of pleiotropy, can reproduce the experimentally observed competition between different cohorts of mutations, some of which have a high probability of fixation along the adaptive walk. Overall, our results show that the surprising dynamics of mutation cohorts recently observed during experimental adaptation of microbial populations can be expected under one of the oldest and simplest theoretical models of adaptation-FGM.

Sex Allocation: L'Enfer C'est les Autres?

Brine shrimp produce a maladaptive excess of sons when co-occurring with females from a related parthenogenetic species. Still, this sex ratio may be adaptive if, by mating with females of the other species, males miss out on mating with their own.

Haplodiploidy and the evolution of eusociality: worker revolution.

Hamilton suggested that inflated relatedness between sisters promotes the evolution of eusociality in haplodiploid populations. Trivers and Hare observed that for this to occur, workers have to direct helping preferentially toward the production of sisters. Building on this, they proposed two biological scenarios whereby haplodiploidy could act to promote the evolution of eusociality: (a) workers biasing the sex allocation of the queen's brood toward females and (b) workers replacing the queen's sons with their own sons. This "worker revolution," whereby the worker class seizes control of sex allocation and reproduction, is expected to lead to helping being promoted in worker-controlled colonies. Here, we use a kin-selection approach to model the two scenarios suggested by Trivers and Hare. We show that (1) worker control of sex allocation may promote helping, but this effect is likely to be weak and short lived; and (2) worker reproduction tends to inhibit rather than promote helping. Furthermore, the promotion of helping is reduced by a number of biologically likely factors, including the presence of workers increasing colony productivity, workers being unmated, and worker control of sex allocation being underpinned by many loci each having a small effect. Overall, our results suggest that haplodiploidy has had a negligible influence on the evolution of eusociality.

Haplodiploidy and the evolution of eusociality: worker reproduction.

Hamilton's haplodiploidy hypothesis suggests that the relatively higher relatedness of full sisters in haplodiploid populations promotes altruistic sib rearing and, consequently, the evolution of eusociality. This haplodiploidy effect works when some broods have a relatively female-biased sex ratio and other broods have a relatively male-biased sex ratio, termed split sex ratios. There is empirical evidence for two scenarios having potentially led to split sex ratios en route to eusociality: unmated queens and queen replacement. A recent analysis of these two scenarios has suggested that haplodiploidy can either promote or inhibit the evolution of eusociality and that the effect is usually small. However, this work made the simplifying assumptions that there is only negligible reproduction by workers and that their offspring have the same sex ratio as those produced by the queen. Here, we relax these assumptions and find that worker reproduction has a negative influence on the evolution of helping, either reducing the extent to which it is promoted or leading to it being inhibited. This is particularly so when workers are unmated and hence constrained to produce only sons, by arrhenotoky. Overall, when parameterized with empirical data, our results suggest that split sex ratios in haplodiploid species have not played an important role in facilitating the evolution of eusociality.

Haplodiploidy and the evolution of eusociality: split sex ratios.

It is generally accepted that from a theoretical perspective, haplodiploidy should facilitate the evolution of eusociality. However, the "haplodiploidy hypothesis" rests on theoretical arguments that were made before recent advances in our empirical understanding of sex allocation and the route by which eusociality evolved. Here we show that several possible promoters of the haplodiploidy effect would have been unimportant on the route to eusociality, because they involve traits that evolved only after eusociality had become established. We then focus on two biological mechanisms that could have played a role: split sex ratios as a result of either queen virginity or queen replacement. We find that these mechanisms can lead haplodiploidy to facilitating the evolution of helping but that their importance varies from appreciable to negligible, depending on the assumptions. Furthermore, under certain conditions, haplodiploidy can even inhibit the evolution of helping. In contrast, we find that the level of promiscuity has a strong and consistently negative influence on selection for helping. Consequently, from a relatedness perspective, monogamy is likely to have been a more important driver of eusociality than the haplodiploidy effect.

Inclusive fitness theory and eusociality.

Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.

Sex and death: the effects of innate immune factors on the sexual reproduction of malaria parasites.

Malaria parasites must undergo a round of sexual reproduction in the blood meal of a mosquito vector to be transmitted between hosts. Developing a transmission-blocking intervention to prevent parasites from mating is a major goal of biomedicine, but its effectiveness could be compromised if parasites can compensate by simply adjusting their sex allocation strategies. Recently, the application of evolutionary theory for sex allocation has been supported by experiments demonstrating that malaria parasites adjust their sex ratios in response to infection genetic diversity, precisely as predicted. Theory also predicts that parasites should adjust sex allocation in response to host immunity. Whilst data are supportive, the assumptions underlying this prediction - that host immune responses have differential effects on the mating ability of males and females - have not yet been tested. Here, we combine experimental work with theoretical models in order to investigate whether the development and fertility of male and female parasites is affected by innate immune factors and develop new theory to predict how parasites' sex allocation strategies should evolve in response to the observed effects. Specifically, we demonstrate that reactive nitrogen species impair gametogenesis of males only, but reduce the fertility of both male and female gametes. In contrast, tumour necrosis factor-α does not influence gametogenesis in either sex but impairs zygote development. Therefore, our experiments demonstrate that immune factors have complex effects on each sex, ranging from reducing the ability of gametocytes to develop into gametes, to affecting the viability of offspring. We incorporate these results into theory to predict how the evolutionary trajectories of parasite sex ratio strategies are shaped by sex differences in gamete production, fertility and offspring development. We show that medical interventions targeting offspring development are more likely to be 'evolution-proof' than interventions directed at killing males or females. Given the drive to develop medical interventions that interfere with parasite mating, our data and theoretical models have important implications.

Brain and gonadal aromatase activity and steroid hormone levels in female and polymorphic males of the peacock blenny Salaria pavo.

In the peacock blenny Salaria pavo large males with well-developed secondary sexual characters establish nests and attract females while small "sneaker" males mimic female sexual displays in order to approach the nests of larger males and parasitically fertilize eggs. These alternative reproductive tactics are sequential, as sneakers irreversibly switch into nesting males. This transition involves major morphologic and behavioral changes and is likely to be mediated by hormones. This study focuses on the role of aromatase, an enzyme that catalyses the conversion of androgens into estrogens, in the regulation of male sexual polymorphism in S. pavo. For this, sex steroid plasma levels and aromatase activity (AA) in gonads, whole brain and brain macroareas were determined in sneakers, transitional males (i.e. sneakers undergoing the transition into nesting males), nesting males and females collected in the field. AA was much higher in ovarian tissue than in testicular tissue and accordingly circulating estradiol levels were highest in females. This supports the view that elevated AA and estradiol levels are associated with the development of a functional ovary. Transitional males are in a non-reproductive phase and had underdeveloped testes when compared with sneakers and nesting males. Testicular AA was approximately 10 times higher in transitional males when compared with sneakers and nesting males, suggesting high AA has a suppressive effect on testicular development. Nesting males had significantly higher plasma levels of both testosterone (T) and 11-ketotestosterone when compared with the other male morphs and previous studies demonstrated that these androgens suppress female-like displays in sneakers. In the brain, AA was highest in macroareas presumably containing hypothalamic nuclei traditionally associated with the regulation of reproductive behaviors. Overall, females presented the highest levels of brain AA. In male morphs AA increased from sneakers, to transitional males, to nesting males in all brain macroareas. These results suggest that the transition into the nesting male tactic is accompanied both by an increase in testicular androgen production and by a higher conversion of androgens into estrogens in the brain. The increase in androgen production is likely to mediate the development of male secondary sexual characters while the increase in brain AA may be related to the behavioral changes associated with tactic transition.

Endocrine control of sexual behavior in sneaker males of the peacock blenny Salaria pavo: effects of castration, aromatase inhibition, testosterone and estradiol.

The effects of castration and sex steroid manipulations on the expression of sexual behavior were investigated in a small fish, the peacock blenny, Salaria pavo. In this species, large males defend nests and attract females while small "sneaker" males reproduce by imitating the female morphology and courtship behavior in order to approach nests during spawning events and parasitically fertilize eggs. Sneakers switch into nest holders in their second breeding season, thus displaying both male and female-like sexual behavior during their lifetime. We tested the effects of castration and of an aromatase inhibitor (Fadrozole, F), testosterone (T) or 17beta-estradiol (E(2)) implants on the expression of male and female-like behavior in sneakers. Sneakers were either sham-operated, castrated or castrated and implanted with vehicle, F, T+F or E(2)+F. Seven days after the treatment, sneakers were placed in a tank with a nesting male, two ripe females and an available nest. Castrated fish had lower levels of circulating T and increased the time spent displaying female typical nuptial coloration. T implants had the opposite effect, inhibiting the expression of female-like behavior and coloration. E(2) implants had no significant effect on the display of sexual behavior but the frequency of aggressive displays decreased. The results agree with previous findings in sneakers of S. pavo that demonstrated an inhibition of female-like behavior by 11-ketotestosterone (11-KT). The reported increase in T and 11-KT production when sneakers change into nest holders may thus contribute to behaviorally defeminize sneakers. Contrarily, both T and E(2) failed to promote male-like behavior, suggesting that behavioral masculization during tactic switching depends on other neuroendocrine mechanisms or that the time length of the experiment was insufficient to induce male-like behavioral changes in sneakers.