Ido Pen

Geographical patterns of adaptation within a species' range: interactions between drift and gene flow

We use individual‐based stochastic simulations and analytical deterministic predictions to investigate the interaction between drift, natural selection and gene flow on the patterns of local adaptation across a fragmented species’ range under clinally varying selection. Migration between populations follows a stepping‐stone pattern and density decreases from the centre to the periphery of the range. Increased migration worsens gene swamping in small marginal populations but mitigates the effect of drift by replenishing genetic variance and helping purge deleterious mutations. Contrary to the deterministic prediction that increased connectivity within the range always inhibits local adaptation, simulations show that low intermediate migration rates improve fitness in marginal populations and attenuate fitness heterogeneity across the range. Such migration rates are optimal in that they maximize the total mean fitness at the scale of the range. Optimal migration rates increase with shallower environmental gradients, smaller marginal populations and higher mutation rates affecting fitness.

Towards a unified theory of cooperative breeding: the role of ecology and life history re-examined

We present quantitative models that unify several adaptive hypotheses for the evolution of cooperative breeding in a single framework: the ecological constraints hypothesis, the life–history hypothesis and the benefits–of–philopatry hypothesis. Our goal is to explain interspecific variation in the occurrence of cooperative breeding in terms of interspecific variation in life–history traits and ecological conditions. We analyse two models, according to whether or not helpers can inherit their parents territory. Major results are (i) territory inheritance always promotes cooperative breeding; (ii) if territories are not inherited, neither ecological constraints nor variation in life–history traits predict interspecific variation in cooperative breeding; and (iii) if territories are inherited, the mechanism of density regulation is crucial in determining which factors promote cooperative breeding. If density dependence acts on the probability to obtain a free territory or on the survival of dispersers, variation in ecological constraints cannot explain variation in cooperative breeding. Lower adult mortality favours helping, not because it reduces the availability of free territories, but because it enhances the direct benefits of helpers. If density dependence acts on fecundity, lower probability of obtaining a free territory and lower survival of dispersers promote cooperative breeding. In this case, lower adult mortality works against the evolution of helping. We suggest that the difference between birds and social insects in the covariance between cooperative breeding and life–history traits is due to different mechanisms of density regulation that operate in these taxa, and we explain how natural selection on habitat choice might have caused these different mechanisms to operate.

Climate-driven population divergence in sex-determining systems

Sex determination is a fundamental biological process, yet its mechanisms are remarkably diverse. In vertebrates, sex can be determined by inherited genetic factors or by the temperature experienced during embryonic development. However, the evolutionary causes of this diversity remain unknown. Here we show that live-bearing lizards at different climatic extremes of the species’ distribution differ in their sex-determining mechanisms, with temperature-dependent sex determination in lowlands and genotypic sex determination in highlands. A theoretical model parameterized with field data accurately predicts this divergence in sex-determining systems and the consequence thereof for variation in cohort sex ratios among years. Furthermore, we show that divergent natural selection on sex determination across altitudes is caused by climatic effects on lizard life history and variation in the magnitude of between-year temperature fluctuations. Our results establish an adaptive explanation for intra-specific divergence in sex-determining systems driven by phenotypic plasticity and ecological selection, thereby providing a unifying framework for integrating the developmental, ecological and evolutionary basis for variation in vertebrate sex determination.

Sex Ratios under Asymmetrical Local Mate Competition: Theory and a Test with Parasitoid Wasps

Sex ratio theory allows unparalleled opportunities for testing how well animal behavior can be predicted by evolutionary theory. For example, Hamilton’s theory of local mate competition (LMC) is well understood and can explain variation in sex allocation across numerous species. This allows more specific predictions to be developed and tested. Here we extend LMC theory to a situation that will be common in a range of species: asymmetrical LMC. Asymmetrical LMC occurs when females lay eggs on a patch asynchronously and male offspring do not disperse, leading to relatively weaker LMC for males emerging from later broods. Varying levels of LMC then lead to varying optimal sex ratios for females, depending on when and where they oviposit. We confirm the assumptions of our theory using the wasp Nasonia vitripennis and then test our predictions. We show that females adjust their offspring sex ratios in the directions predicted, laying different sex ratios on different hosts within a patch. Specifically, there was a less female‐biased sex ratio when ovipositing on an unparasitized host if another host on the patch had previously been parasitized and a less female‐biased sex ratio on parasitized hosts if females also oviposited on an unparasitized host.

Three epigenetic information channels and their different roles in evolution

There is increasing evidence for epigenetically mediated transgenerational inheritance across taxa. However, the evolutionary implications of such alternative mechanisms of inheritance remain unclear. Herein, we show that epigenetic mechanisms can serve two fundamentally different functions in transgenerational inheritance: (i) selection‐based effects, which carry adaptive information in virtue of selection over many generations of reliable transmission; and (ii) detection‐based effects, which are a transgenerational form of adaptive phenotypic plasticity. The two functions interact differently with a third form of epigenetic information transmission, namely information about cell state transmitted for somatic cell heredity in multicellular organisms. Selection‐based epigenetic information is more likely to conflict with somatic cell inheritance than is detection‐based epigenetic information. Consequently, the evolutionary implications of epigenetic mechanisms are different for unicellular and multicellular organisms, which underscores the conceptual and empirical importance of distinguishing between these two different forms of transgenerational epigenetic effect.

Sex-ratio optimization with helpers at the nest

In many cooperatively breeding animals, offspring produced earlier in life assist their parents in raising subsequent broods. Such helping behaviour is often confined to offspring of one sex. Sex-allocation theory predicts that parents overproduce offspring of the helping sex, but the expected degree of sex-ratio bias was thought to depend on specific details of female and male life histories, hampering empirical tests of the theory. Here we demonstrate the following two theories. (i) If all parents produce the same sex ratio, the evolutionarily stable sex ratio obeys a very simple rule that is valid for a general class of life histories. The rule predicts that the expected sex-ratio bias depends on the product of only two parameters which are relatively easily measured: the average number of helping offspring per nest and the relative contribution to offspring production per helper. (ii) If the benefit of helping varies between parents, and parents facultatively adjust the sex ratio accordingly, then the population sex ratio is not necessarily biased towards the helping sex. For example, in line with empirical evidence, if helpers are produced under favourable conditions and parents do not adjust their clutch size to the number of helpers, then a surplus of the non-helping sex is expected.

Kin discrimination and sex ratios in a parasitoid wasp

Sex ratio theory provides a clear and simple way to test if nonsocial haplodiploid wasps can discriminate between kin and nonkin. Specifically, if females can discriminate siblings from nonrelatives, then they are expected to produce a higher proportion of daughters if they mate with a sibling. This prediction arises because in haplodiploids, inbreeding (sib‐mating) causes a mother to be relatively more related to her daughters than her sons. Here we formally model this prediction for when multiple females lay eggs in a patch, and test it with the parasitoid wasp Nasonia vitripennis. Our results show that females do not adjust their sex ratio behaviour dependent upon whether they mate with a sibling or nonrelative, in response to either direct genetic or a range of indirect environmental cues. This suggests that females of N. vitripennis cannot discriminate between kin and nonkin. The implications of our results for the understanding of sex ratio and social evolution are discussed.

Genomic conflict in scale insects: the causes and consequences of bizarre genetic systems.

It is now clear that mechanisms of sex determination are extraordinarily labile, with considerable variation across all taxonomic levels. This variation is often expressed through differences in the genetic system (XX‐XY, XX‐XO, haplodiploidy, and so on). Why there is so much variation in such a seemingly fundamental process has attracted much attention, with recent ideas concentrating on the possible role of genomic conflicts of interest. Here we consider the role of inter‐ and intra‐genomic conflicts in one large insect taxon: the scale insects. Scale insects exhibit a dizzying array of genetic systems, and their biology promotes conflicts of interest over transmission and sex ratio between male‐ and female‐expressed genes, parental‐ and offspring‐expressed genes (both examples of intra‐genomic conflict) and between scale insects and their endosymbionts (inter‐genomic conflict). We first review the wide range of genetic systems found in scale insects and the possible evolutionary transitions between them. We then outline the theoretical opportunities for genomic conflicts in this group and how these might influence sex determination and sex ratio. We then consider the evidence for these conflicts in the evolution of sex determination in scale insects. Importantly, the evolution of novel genetic systems in scale insects has itself helped create new conflicts of interest, for instance over sex ratio. As a result, a major obstacle to our understanding of the role of conflict in the evolution of sex‐determination and genetic systems will be the difficulty in identifying the direction of causal relationships. We conclude by outlining possible experimental and comparative approaches to test more effectively how important genomic conflicts have been.

Sex ratio selection and multi-factorial sex determination in the housefly: a dynamic model

Sex determining (SD) mechanisms are highly variable between different taxonomic groups and appear to change relatively quickly during evolution. Sex ratio selection could be a dominant force causing such changes. We investigate theoretically the effect of sex ratio selection on the dynamics of a multi‐factorial SD system. The system considered resembles the naturally occurring three‐locus system of the housefly, which allows for male heterogamety, female heterogamety and a variety of other mechanisms. Sex ratio selection is modelled by assuming cost differences in the production of sons and daughters, a scenario leading to a strong sex ratio bias in the absence of constraints imposed by the mechanism of sex determination. We show that, despite of the presumed flexibility of the SD system considered, equilibrium sex ratios never deviate strongly from 1 : 1. Even if daughters are very costly, a male‐biased sex ratio can never evolve. If sons are more costly, sex ratio can be slightly female biased but even in case of large cost differences the bias is very small (<10% from 1 : 1). Sex ratio selection can lead to a shift in the SD mechanism, but cannot be the sole cause of complete switches from one SD system to another. In fact, more than one locus remains polymorphic at equilibrium. We discuss our results in the context of evolution of the variable SD mechanism found in natural housefly populations.

Seasonal Sex Ratio Trend in the European Kestrel: An Evolutionarily Stable Strategy Analysis

We present an evolutionarily stable strategy (ESS) model to analyze selection on seasonal variation in the brood sex ratio, as observed in several species of raptorial birds. The model is specifically tailored to the life history of the European kestrel, and it reflects the maturation time hypothesis, the idea that a seasonal sex ratio trend has evolved because of sex differences in the dependence of age of first breeding on date of birth. First we show how to derive a fitness function in the context of a seasonal environment. Model parameters are estimated from field data in order to derive quantitative predictions. Since little is known about constraints on sex ratio control in birds, we analyze three scenarios, each corresponding to a different strategy set. We consider a model without constraints on sex ratio control, a model where the sex ratio trend is constrained to be linear, and a mechanistic model incorporating a plausible mechanism of sex ratio control in birds. One of the models yields an ESS sex ratio trend that closely resembles the trend observed in the field. However, the predictions are very sensitive to the choice of strategy set. Moreover, the selective forces generated by sex differences in maturation are rather weak. In fact, the mechanistic model shows that seemingly negligible costs of sex ratio control may be sufficient to overcome the adaptive value of adjusting the sex ratio.