Parental age can have considerable effects on offspring phenotypes and health. However, intergenerational effects may also have longer term effects on offspring fitness. Few studies have investigated parental age effects on offspring fitness in natural populations while also testing for sex‐ and environment‐specific effects. Further, longitudinal parental age effects may be masked by population‐level processes such as the selective disappearance of poor‐quality individuals. Here, we used multigenerational data collected on individually marked Seychelles warblers (Acrocephalus sechellensis) to investigate the impact of maternal and paternal age on offspring life span and lifetime reproductive success. We found negative effects of maternal age on female offspring life span and lifetime reproductive success, which were driven by within‐mother effects. There was no difference in annual reproductive output of females born to older versus younger mothers, suggesting that the differences in offspring lifetime reproductive success were driven by effects on offspring life span. In contrast, there was no association between paternal age and female offspring life span or either maternal or paternal age and male offspring life span. Lifetime reproductive success, but not annual reproductive success, of male offspring increased with maternal age, but this was driven by between‐mother effects. No paternal age effects were found on female offspring lifetime reproductive success but there was a positive between‐father effect on male offspring lifetime reproductive success. We did not find strong evidence for environment‐dependent parental age effects. Our study provides evidence for parental age effects on the lifetime fitness of offspring and shows that such effects can be sex dependent. These results add to the growing literature indicating the importance of intergenerational effects on long‐term offspring performance and highlight that these effects can be an important driver of variation in longevity and fitness in the wild.

Interactions between species are widely understood to have promoted the diversification of life on Earth, but how interactions spur the formation of new species remains unclear. Interacting species often become locally adapted to each other, but they may also be subject to shared dispersal limitations and environmental conditions. Moreover, theory predicts that different kinds of interactions have different effects on diversification. To better understand how species interactions promote diversification, we compiled population genetic studies of host plants and intimately associated herbivores, parasites, and mutualists. We used Bayesian multiple regressions and the BEDASSLE modeling framework to test whether host and associate population structures were correlated over and above the potentially confounding effects of geography and shared environmental variation. We found that associates' population structure often paralleled their hosts' population structure, and that this effect is robust to accounting for geographic distance and climate. Associate genetic structure was significantly explained by plant genetic structure somewhat more often in antagonistic interactions than in mutualistic ones. This aligns with a key prediction of coevolutionary theory that antagonistic interactions promote diversity through local adaptation of antagonists to hosts, while mutualistic interactions more often promote diversity via the effect of hosts' geographic distribution on mutualists' dispersal.

Impact Summary Females and males are dimorphic for a wide range of traits, including the average lengths of their life spans. Sex differences in life span are both conspicuous and variable among species. For example, in mammals, females live ∼20% longer than males (on average), whereas in birds, males live ∼10% longer than females. One leading explanation for these patterns—the unguarded X hypothesis—argues that sex differences in life span emerge from the distinct sex chromosomes that females and males inherit. For many species, one sex (e.g., female mammals; male birds) carries two copies of each X-linked gene, whereas the other carries one. Because harmful mutations are partially recessive, the sex with only one copy of the X is more prone to expressing them, and that sex should therefore have a shorter average life span. This prediction of the unguarded X hypothesis is qualitatively consistent with observations of sex-ratio bias in adults and sexual dimorphism for longevity (e.g., mammalian males have one copy of the X and have shorter lives than females). However, there are other possible explanations for these patterns, making it unclear how much the unguarded X explains species diversity for sex-specific longevity. We developed a mathematical model for the contribution of unguarded X effects to sex differences in survival and life span, and used data on mutation rates and their effects on survival and fitness to quantify the importance of the unguarded X across species. The model, when combined with current data, suggests that the unguarded X hypothesis cannot explain the conspicuous sex differences in life span that are commonly reported in animal species, particularly vertebrates. Our results suggest that the unguarded X is an unlikely general explanation for the evolution of sexually dimorphic life spans, which gives weight to alternative mechanisms, including “toxic Y” effects and sex differential selection via trade-offs between survival and reproduction.

Reproductive parasites such as Wolbachia spread within host populations by inducing cytoplasmic incompatibility (CI). CI occurs when parasite‐modified sperm fertilizes uninfected eggs and is typified by great variation in strength across biological systems. In haplodiploid hosts, CI has different phenotypic outcomes depending on whether the fertilized eggs die or develop into males. Genetic conflict theories predict the evolution of host modulation of CI, which in turn influences the stability of reproductive parasitism. However, despite the ubiquity of CI‐inducing parasites in nature, there is scarce evidence for intraspecific host modulation of CI strength and phenotype. Here, we tested for intraspecific host modulation of Wolbachia‐induced CI in haplodiploid Tetranychus urticae mites. Using a single CI‐inducing Wolbachia variant and mitochondrion, a nuclear panel was created that consisted of infected and cured near‐isogenic lines. We performed a highly replicated age‐synchronized full diallel cross composed of incompatible and compatible control crosses. We uncovered host modifier systems that cause striking variation in CI strength when carried by infected T. urticae males. We observed a continuum of CI phenotypes in our crosses and identified strong intraspecific female modulation of the CI phenotype. Crosses established a recessive genetic basis for the maternal effect and were consistent with polygenic Mendelian inheritance. Both male and female modulation interacted with the genotype of the mating partner. Our findings identify spermatogenesis as an important target of selection for host modulation of CI strength and underscore the importance of maternal genetic effects for the CI phenotype. Our findings reveal that intraspecific host modulation of CI is underpinned by complex genetic architectures and confirm that the evolution of reproductive parasitism is contingent on host genetics.

The mismatch between when individuals breed and when we think they should breed has been a long‐standing problem in evolutionary ecology. Price et al. is a classic theory paper in this field and is mainly cited for its most obvious result: if individuals with high nutritional condition breed early, then the advantage of breeding early may be overestimated when information on nutritional condition is absent. Price at al.'s less obvious result is that individuals, on average, are expected to breed later than the optimum. Here, we provide an explanation of their non‐intuitive result in terms of hard selection, and go on to show that neither of their results are expected to hold if the relationship between breeding date and nutrition is allowed to evolve. By introducing the assumption that the advantage of breeding early is greater for individuals in high nutritional condition, we show that their most cited result can be salvaged. However, individuals, on average, are expected to breed earlier than the optimum, not later. More generally, we also show that the hard selection mechanisms that underpin these results have major implications for the evolution of plasticity: when environmental heterogeneity becomes too great, plasticity is selected against, prohibiting the evolution of generalists.

Maternally inherited Wolbachia transinfections are being introduced into natural mosquito populations to reduce the transmission of dengue, Zika, and other arboviruses. Wolbachia-induced cytoplasmic incompatibility provides a frequency-dependent reproductive advantage to infected females that can spread transinfections within and among populations. However, because transinfections generally reduce host fitness, they tend to spread within populations only after their frequency exceeds a critical threshold. This produces bistability with stable equilibrium frequencies at both 0 and 1, analogous to the bistability produced by underdominance between alleles or karyotypes and by population dynamics under Allee effects. Here, we analyze how stochastic frequency variation produced by finite population size can facilitate the local spread of variants with bistable dynamics into areas where invasion is unexpected from deterministic models. Our exemplar is the establishment of wMel Wolbachia in the Aedes aegypti population of Pyramid Estates (PE), a small community in far north Queensland, Australia. In 2011, wMel was stably introduced into Gordonvale, separated from PE by barriers to A. aegypti dispersal. After nearly 6 years during which wMel was observed only at low frequencies in PE, corresponding to an apparent equilibrium between immigration and selection, wMel rose to fixation by 2018. Using analytic approximations and statistical analyses, we demonstrate that the observed fixation of wMel at PE is consistent with both stochastic transition past an unstable threshold frequency and deterministic transformation produced by steady immigration at a rate just above the threshold required for deterministic invasion. The indeterminacy results from a delicate balance of parameters needed to produce the delayed transition observed. Our analyses suggest that once Wolbachia transinfections are established locally through systematic introductions, stochastic "threshold crossing" is likely to only minimally enhance spatial spread, providing a local ratchet that slightly-but systematically-aids area-wide transformation of disease-vector populations in heterogeneous landscapes.

Genetic diversity varies among species due to a range of eco‐evolutionary processes that are not fully understood. The neutral theory predicts that the amount of variation in the genome sequence between different individuals of the same species should increase with its effective population size (Ne). In real populations, multiple factors that modulate the variance in reproductive success among individuals cause Ne to differ from the total number of individuals (N). Among these, age‐specific mortality and fecundity rates are known to have a direct impact on the Ne/N ratio. However, the extent to which vital rates account for differences in genetic diversity among species remains unknown. Here, we addressed this question by comparing genome‐wide genetic diversity across 16 marine fish species with similar geographic distributions but contrasted lifespan and age‐specific survivorship and fecundity curves. We sequenced the whole genome of 300 individuals to high coverage and assessed their genome‐wide heterozygosity with a reference‐free approach. Genetic diversity varied from 0.2% to 1.4% among species, and showed a negative correlation with adult lifespan, with a large negative effect (slope=−0.089 per additional year of lifespan) that was further increased when brooding species providing intense parental care were removed from the dataset (slope=−0.129 per additional year of lifespan). Using published vital rates for each species, we showed that the Ne/N ratio resulting simply from life tables parameters can predict the observed differences in genetic diversity among species. Using simulations, we further found that the extent of reduction in Ne/N with increasing adult lifespan is particularly strong under Type III survivorship curves (high juvenile and low adult mortality) and increasing fecundity with age, a typical characteristic of marine fishes. Our study highlights the importance of vital rates as key determinants of species genetic diversity levels in nature.

Evolutionary innovations can facilitate diversification if the novel trait enables a lineage to exploit new niches or by expanding character space. The elaborate pharyngeal jaw apparatus of cichlid fishes is often referred to as an evolutionary “key innovation” that has promoted the spectacular adaptive radiations in these fishes. This goes back to the idea that the structural and functional independence of the oral and pharyngeal jaws for food capturing and food processing, respectively, permitted each jaw type to follow independent evolutionary trajectories. This “evolutionary decoupling” is thought to have facilitated novel trait combinations and, hence, ecological specialization, ultimately allowing more species to coexist in sympatry. Here, we test the hypotheses of evolutionary decoupling of the oral and pharyngeal jaws in the massive adaptive radiation of cichlid fishes in African Lake Tanganyika. Based on phylogenetic comparative analyses of oral jaw morphology and lower pharyngeal jaw shape across most of the ∼240 cichlid species occurring in that lake, we show that the two jaws evolved coupled along the main axes of morphological variation, yet most other components of these trait complexes evolved largely independently over the course of the radiation. Further, we find limited correlations between the two jaws in both overall divergence and evolutionary rates. Moreover, we show that the two jaws were evolutionary decoupled at a late stage of the radiation, suggesting that decoupling contributed to micro‐niche partitioning and the associated rapidly increasing trophic diversity during this phase.

Whether females should prefer to mate with old males is controversial. Old males may sire offspring of low quality because of an aging germline, but their proven ability to reach an old age can also be an excellent indicator of superior genetic quality, especially in natural populations. These genetic effects are, however, hard to study in nature, because they are often confounded with direct benefits offered by old males to the female, such as experience and high territory quality. We, therefore, used naturally occurring extra‐pair young to disentangle different aspects of male age on female fitness in a natural population of collared flycatchers because any difference between within‐ and extra‐pair young within a nest should be caused by paternal genetic effects only. Based on 18 years of long‐term data, we found that females paired with older males as social partners experienced an overall reproductive advantage. However, offspring sired by old males were of lower quality as compared to their extra‐pair half‐siblings, whereas the opposite was found in nests attended by young males. These results imply a negative genetic effect of old paternal age, given that extra‐pair males are competitive middle‐age males. Thus, offspring may benefit from being sired by young males but raised by old males, to maximize both genetic and direct effects. Our results show that direct and genetic benefits from pairing with old males may act in opposing directions and that the quality of the germline may deteriorate before other signs of senescence become obvious.