Context‐dependent effects of Y chromosome and mitochondrial haplotype on male locomotive activity in Drosophila melanogaster

Some regions of the genome exhibit sexual asymmetries in inheritance and are thus subjected to sex‐biased evolutionary forces. Maternal inheritance of mitochondrial DNA (mtDNA) enables mtDNA mutations harmful to males, but not females, to accumulate. In the face of male‐harmful mtDNA mutation accumulation, selection will favour the evolution of compensatory modifiers in the nuclear genome that offset fitness losses to males. The Y chromosome is a candidate to host these modifiers, because it is paternally inherited, known to harbour an abundance of genetic variation for male fertility, and therefore likely to be under strong selection to uphold male viability. Here, we test for intergenomic interactions involving mtDNA and Y chromosomes in male Drosophila melanogaster. Specifically, we examine effects of each of these genomic regions, and their interaction, on locomotive activity, across different environmental contexts – both dietary and social. We found that both the mtDNA haplotype and Y chromosome haplotype affected activity in males assayed in an environment perceived as social. These effects, however, were not evident in males assayed in perceived solitary environments, and neither social nor solitary treatments revealed evidence for intergenomic interactions. Finally, the magnitude and direction of these genetic effects was further contingent on the diet treatment of the males. Thus, genes within the mtDNA and Y chromosome are involved in genotype‐by‐environment interactions. These interactions might contribute to the maintenance of genetic variation within these asymmetrically inherited gene regions and complicate the dynamics of genetic interactions between the mtDNA and the Y chromosome.     

Sex‐specific heritability of cell‐mediated immune response in the blue tit nestlings (Cyanistes caeruleus)

Here, we aimed at estimating sex‐specific heritabilities of cell‐mediated immune response (CMI) in the blue tit nestlings (Cyanistes caeruleus). To separate genetic and environmental components of the phenotypic variance in CMI (measured using phytohaemagglutinin assay), we performed a cross‐fostering experiment. Additionally, controlled environmental variation was introduced by enlarging some broods. Our analyses revealed a significant genetic component (as approximated by the nest‐of‐origin term) of the phenotypic variance in immune response. More importantly, these genetic effects differed between sexes and experimentally manipulated brood sizes, as indicated by significant genotype‐by‐sex and genotype‐by‐environment interactions. We discuss possible causes of such sexual dimorphism in gene expression and suggest that sex‐ and environment‐specific genetic interactions may contribute to the maintenance of genetic variability in traits related to immune functions.     

Genetic by environment interactions affect plant–soil linkages

The role of plant intraspecific variation in plant–soil linkages is poorly understood, especially in the context of natural environmental variation, but has important implications in evolutionary ecology. We utilized three 18‐ to 21‐year‐old common gardens across an elevational gradient, planted with replicates of five Populus angustifolia genotypes each, to address the hypothesis that tree genotype (G), environment (E), and G × E interactions would affect soil carbon and nitrogen dynamics beneath individual trees. We found that soil nitrogen and carbon varied by over 50% and 62%, respectively, across all common garden environments. We found that plant leaf litter (but not root) traits vary by genotype and environment while soil nutrient pools demonstrated genotype, environment, and sometimes G × E interactions, while process rates (net N mineralization and net nitrification) demonstrated G × E interactions. Plasticity in tree growth and litter chemistry was significantly related to the variation in soil nutrient pools and processes across environments, reflecting tight plant–soil linkages. These data overall suggest that plant genetic variation can have differential affects on carbon storage and nitrogen cycling, with implications for understanding the role of genetic variation in plant–soil feedback as well as management plans for conservation and restoration of forest habitats with a changing climate.     

Maternal influences on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination

Maternal and environmental factors are important sources of phenotypic variation because both factors influence offspring traits in ways that impact offspring and maternal fitness. The present study explored the effects of maternal factors (maternal body size, egg size, yolk‐steroid allocation, and oviposition‐site choice) and seasonally‐variable environmental factors on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination (Amphibolurus muricatus). Maternal identity had strong effects on offspring morphology, but the nature of maternal effects differed among successive clutches produced by females throughout the reproductive season (i.e. maternal identity by environment interactions). The among‐female and among‐clutch variation in offspring traits (including sex ratios) was not mediated through maternal body size, egg size, or variation in yolk steroid hormones. This lack of nongenetic maternal effects suggests that phenotypic variation may be generated by gene by environment interactions. These results demonstrate a significant genetic component to variation in offspring phenotypes, including sex ratios, even in species with environmental sex determination. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 256–266.     

Disentangling the effects of genetic and environmental factors on movement behaviour

Individual variability in animal movement behaviour is well documented for many species. However, it remains unclear whether this variability reflects genetic variation, environmental variation or a combination of the two. Here, we conduct a cross‐fostering experiment with the aim of investigating the role of these two components in movement patterns during the post‐fledging dependence period and early natal dispersal of 21 eagle owls Bubo bubo. Our experiment showed that cross‐fostering did not influence any of the movement parameters considered. Movement parameters were, however, affected by the age and sex of the owlets. We therefore suggest that individual variability and family resemblance in movement behaviour during the post‐fledging dependence period and early natal dispersal might not be due to the common genetic origin of siblings, but rather that it originates from factors related to the rearing environment.     

Heritability of male attractiveness persists despite evidence for unreliable sexual signals in Drosophila simulans

Sexual signals can be used to attract mates, but to be honest indicators of signaller quality they need to convey information reliably. However, environmental variation and genotype‐by‐environment (G × E) interactions have the potential to compromise the reliability of sexual signals. Here, we test the reliability of cuticular hydrocarbons (CHCs) as signals of heritable aspects of male attractiveness in Drosophila simulans. We examined the heritability of male attractiveness and a measure of the difference between fathers' and sons' CHC profiles across dietary and temperature environments. Our results show that environmental heterogeneity disrupts the similarity of some components of father and son CHC profile. However, overall male attractiveness is heritable within and across environments, so that sire attractiveness is a good predictor of son attractiveness even with environmental heterogeneity. This suggests that although some male CHC signals are unreliable, attractive genotypes retain their attractiveness across environments on average.     

Genotype‐by‐environment interactions for cuticular hydrocarbon expression in Drosophila simulans

Genotype‐by‐environment interactions (G × Es) describe genetic variation for phenotypic plasticity. Recent interest in the role of these interactions in sexual selection has identified G × Es across a diverse range of species and sexual traits. Additionally, theoretical work predicts that G × Es in sexual traits could help to maintain genetic variation, but could also disrupt the reliability of these traits as signals of mate quality. However, empirical tests of these theoretical predictions are scarce. We reared iso‐female lines of Drosophila simulans across two axes of environmental variation (diet and temperature) in a fully factorial design and tested for G × Es in the expression of cuticular hydrocarbons (CHCs), a multivariate sexual trait in this species. We find sex‐specific environmental, genetic and G × E effects on CHC expression, with G × Es for diet in both male and female CHC profile and a G × E for temperature in females. We also find some evidence for ecological crossover in these G × Es, and by quantifying variance components, genetic correlations and heritabilities, we show the potential for these G × Es to help maintain genetic variation and cause sexual signal unreliability in D. simulans CHC profiles.     

Population differentiation in the beetle Tribolium castaneum. II. Haldane'S rule and incipient speciation

The heterogametic sex tends to be rare, absent, sterile, or deformed in F1 hybrid crosses between species, a pattern called Haldane's rule (HR). The introgression of single genes or chromosomal regions from one drosophilid species into the genetic background of another have shown that HR is most often associated with fixed genetic differences in inter-specific crosses. However, because such introgression studies have involved species diverged several hundred thousand generations from a common ancestor, it is not clear whether HR attends the speciation process or results from the accumulation of epistatically acting genes postspeciation. We report the first evidence for HR prior to speciation in crosses between two populations of the red flour beetle, Tribolium castaneum, collected 931 km apart in Colombia and Ecuador. In this cross, HR is manifested as an increase in the proportion of deformed males compared to females and the expression of HR is temperature dependent. Neither population, when crossed to a geographically distant population from Japan, exhibits HR at any rearing temperature. Using joint-scaling analysis and additional data from backcrosses and F2's, we find that the hybrid incompatibilities and the emergence of HR are concurrent processes involving interactions between X-linked and autosomal genes. However, we also find many examples of incompatibilities manifest by F2 and backcross hybrids but not by F1 hybrids and most incompatibilities are not sex different in their effects, even when they involve both X-autosomal interactions and genotype-by-environment interactions. We infer that incipient speciation in flour beetles can occur with or without HR and that significant hybrid incompatibilities result from the accumulation of epistatically acting gene differences between populations without differentially affecting the heterogametic sex in F1 hybrids. The temperature dependence of the incompatibilities supports the inference that genotype-by-environment interactions and adaptation to different environments contribute to the genetic divergence important to postzygotic reproductive isolation.     

Survival rates indicate that correlations between community‐weighted mean traits and environments can be unreliable estimates of the adaptive value of traits

Correlations between community‐weighted mean (CWM) traits and environmental gradients are often assumed to quantify the adaptive value of traits. We tested this assumption by comparing these correlations with models of survival probability using 46 perennial species from long‐term permanent plots in pine forests of Arizona. Survival was modelled as a function of trait × environment interactions, plant size, climatic variation and neighbourhood competition. The effect of traits on survival depended on the environmental conditions, but the two statistical approaches were inconsistent. For example, CWM‐specific leaf area (SLA) and soil fertility were uncorrelated. However, survival was highest for species with low SLA in infertile soil, a result which agreed with expectations derived from the physiological trade‐off underpinning leaf economic theory. CWM trait–environment relationships were unreliable estimates of how traits affected survival, and should only be used in predictive models when there is empirical support for an evolutionary trade‐off that affects vital rates.     

The evolution of genetic architecture. I. Diversification of genetic backgrounds by genetic drift

The genetic architecture of a phenotype plays a critical role in determining phenotypic evolution through its effects on patterns of genetic variation. Genetic architecture is often considered to be constant in evolutionary quantitative genetic models. However, genetic architecture may be variable and itself evolve when there are dominance and epistatic interactions among alleles at the same and different loci, respectively. The evolution of genetic architecture by genetic drift is examined here by testing the breeding value of four standard inbred mouse strains mated across a set of 26 related recombinant quasi-inbred (RqI) lines generated from the intercross of the Large (LG/J) and Small (SM/J) inbred mouse strains. Phenotypes of interest include age-specific body weights, growth, and adult body composition. If the genetic architecture of these traits has differentiated by genetic drift during the production of the RqI strains, we should observe interactions between tester strain and RqI strain. The breeding values of the tester strains will change relative to one another depending on which RqI strain they are crossed to. The study included an average of 15.1 offspring per cross, over a total of 100 different crosses. Multivariate and univariate analyses of variance indicate that there is strongly significant interaction for all traits. Interaction is more pronounced in males than in females and accounted for an average of about 40% of the explained variation in males and 30% in females. These results indicate that the genetic architecture of these traits has differentiated by genetic drift in the RqI strains since their isolation from a common founder population. Further analysis indicates that this differentiation results in changes in the order of tester strain effects so that common patterns of selection in these differentiated populations could result in the fixation of different alleles.     

GENETIC ARCHITECTURE OF ISOLATION BETWEEN TWO SPECIES OF SILENE WITH SEX CHROMOSOMES AND HALDANE'S RULE

Examination of the genetic architecture of hybrid breakdown can provide insight into the genetic mechanisms of commonly observed isolating phenomena such as Haldane's rule. We used line‐cross analysis to dissect the genetic architecture of divergence between two plant species that exhibit Haldane's rule for male sterility and rarity, Silene latifolia and Silene diclinis. We made 15 types of crosses, including reciprocal F₁, F₂, backcrosses, and later‐generation crosses, grew the seeds to flowering, and measured the number of viable ovules, proportion of viable pollen, and sex ratio. Typically, Haldane's rule for male rarity in XY animal hybrids is explained by interactions involving recessive X‐linked alleles that are deleterious when hemizygous (dominance theory), whereas sterility is explained by rapid evolution of spermatogenesis genes (faster‐male evolution). In contrast, we found that the genetic mechanisms underlying Haldane's rule between the two Silene species did not follow these conventions. Dominance theory was sufficient to explain male sterility, but male rarity likely involved faster‐male evolution. We also found an effect of the neo‐sex chromosomes of S. diclinis on the extreme rarity of some hybrid males. Our findings suggest that the genetic architecture of Haldane's rule in dioecious plants may differ from those commonly found in animals.     

Risk‐induced hatching timing shows low heritability and evolves independently of spontaneous hatching in red‐eyed treefrogs

Plasticity in the timing of transitions between stages of complex life cycles allows organisms to adjust their growth and development to local environmental conditions. Genetic variation in such plasticity is common, but the evolution of context‐dependent transition timing may be constrained by information reliability, lag‐time and developmental constraints. We studied the genetic architecture of hatching plasticity in embryos of the red‐eyed treefrog (Agalychnis callidryas) in response to simulated predator attacks using a series of paternal and maternal half‐sibs from a captive breeding colony of wild‐collected animals. We compared the developmental timing of induced early hatching across sibships and estimated cross‐environment genetic correlations between induced and spontaneous hatching traits. Additive genetic variance for induced early hatching was very low, indicating a constraint on the short‐term evolution of earlier hatching timing. This constraint is likely related to the maturation of the hatching mechanism. The most plastic genotypes produced the most extreme spontaneous hatching phenotypes, indicating that developmental range, per se, is not constrained. Cross‐environment genetic correlation in hatching timing was negligible, so the evolution of spontaneous hatching in this species has not depended on the evolution of risk‐induced hatching and vice versa.     

Microhabitat selection in the common lizard: implications of biotic interactions,age, sex,local processes,and model transferability among populations

Modeling species' habitat requirements are crucial to assess impacts of global change, for conservation efforts and to test mechanisms driving species presence. While the influence of abiotic factors has been widely examined, the importance of biotic factors and biotic interactions, and the potential implications of local processes are not well understood. Testing their importance requires additional knowledge and analyses at local habitat scale. Here, we recorded the locations of species presence at the microhabitat scale and measured abiotic and biotic parameters in three different common lizard (Zootoca vivipara) populations using a standardized sampling protocol. Thereafter, space use models and cross‐evaluations among populations were run to infer local processes and estimate the importance of biotic parameters, biotic interactions, sex, and age. Biotic parameters explained more variation than abiotic parameters, and intraspecific interactions significantly predicted the spatial distribution. Significant differences among populations in the relationship between abiotic parameters and lizard distribution, and the greater model transferability within populations than between populations are in line with effects predicted by local adaptation and/or phenotypic plasticity. These results underline the importance of including biotic parameters and biotic interactions in space use models at the population level. There were significant differences in space use between sexes, and between adults and yearlings, the latter showing no association with the measured parameters. Consequently, predictive habitat models at the population level taking into account different sexes and age classes are required to understand a specie's ecological requirements and to allow for precise conservation strategies. Our study therefore stresses that future predictive habitat models at the population level and their transferability should take these parameters into account.     

Climate change,sex reversal and lability of sex‐determining systems

Sex reversal at high temperatures during embryonic development (e.g., ZZ females) provides the opportunity for new genotypic crosses (e.g., ZZ male × ZZ female). This raises the alarming possibility that climatic warming could lead to the loss of an entire chromosome—one member of the sex chromosome pair (the Y or W)—and the transition of populations to environmental sex determination (ESD). Here we examine the evolutionary dynamics of sex‐determining systems exposed to climatic warming using theoretical models. We found that the loss of sex chromosomes is not an inevitable consequence of sex reversal. A large frequency of ZZ sex reversal (50% reversal from male to female) typically divides the outcome between loss of the ZW genotype and the stable persistence of ZZ males, ZW females and ZZ females. The amount of warming associated with sex chromosome loss depended on several features of wild populations—environmental fluctuation, immigration, heritable variation in temperature sensitivity and differential fecundity of sex‐reversed individuals. Chromosome loss was partially or completely buffered when sex‐reversed individuals suffered a reproductive fitness cost, when immigration occurred or when heritable variation for temperature sensitivity existed. Thus, under certain circumstances, sex chromosomes may persist cryptically in systems where the environment is the predominant influence on sex.     

Complex mitonuclear interactions and metabolic costs of mating in male seed beetles

The lack of evolutionary response to selection on mitochondrial genes through males predicts the evolution of nuclear genetic influence on male‐specific mitochondrial function, for example by gene duplication and evolution of sex‐specific expression of paralogs involved in metabolic pathways. Intergenomic epistasis may therefore be a prevalent feature of the genetic architecture of male‐specific organismal function. Here, we assess the role of mitonuclear genetic variation for male metabolic phenotypes [metabolic rate and respiratory quotient (RQ)] associated with ejaculate renewal, in the seed beetle Callosobruchus maculatus, by assaying lines with crossed combinations of distinct mitochondrial haplotypes and nuclear lineages. We found a significant increase in metabolic rate following mating relative to virgin males. Moreover, processes associated with ejaculate renewal showed variation in metabolic rate that was affected by mitonuclear interactions. Mitochondrial haplotype influenced mating‐related changes in RQ, but this pattern varied over time. Mitonuclear genotype and the energy spent during ejaculate production affected the weight of the ejaculate, but the strength of this effect varied across mitochondrial haplotypes showing that the genetic architecture of male‐specific reproductive function is complex. Our findings unveil hitherto underappreciated metabolic costs of mating and ejaculate renewal, and provide the first empirical demonstration of mitonuclear epistasis on male reproductive metabolic processes.     

Sex without sex chromosomes: genetic architecture of multiple loci independently segregating to determine sex ratios in the copepod Tigriopus californicus

Sex‐determining systems are remarkably diverse and may evolve rapidly. Polygenic sex‐determination systems are predicted to be transient and evolutionarily unstable, yet examples have been reported across a range of taxa. Here, we provide the first direct evidence of polygenic sex determination in Tigriopus californicus, a harpacticoid copepod with no heteromorphic sex chromosomes. Using genetically distinct inbred lines selected for male‐ and female‐biased clutches, we generated a genetic map with 39 SNPs across 12 chromosomes. Quantitative trait locus mapping of sex ratio phenotype (the proportion of male offspring produced by an F2 female) in four F2 families revealed six independently segregating quantitative trait loci on five separate chromosomes, explaining 19% of the variation in sex ratios. The sex ratio phenotype varied among loci across chromosomes in both direction and magnitude, with the strongest phenotypic effects on chromosome 10 moderated to some degree by loci on four other chromosomes. For a given locus, sex ratio phenotype varied in magnitude for individuals derived from different dam lines. These data, together with the environmental factors known to contribute to sex determination, characterize the underlying complexity and potential lability of sex determination, and confirm the polygenic architecture of sex determination in T. californicus.     

Effects of plant sex on insect abundance across three trophic levels in the perennial shrub Buddleja cordata

Although there is a growing interest in the effects of intra‐specific plant genetic variation on species interactions, the effects of plant sex, an important axis of genetic variation, have been less studied. In addition, previous work investigating plant sex effects on species interactions has frequently focused on bitrophic interactions (e.g., herbivory), usually ignoring plant sex effects on higher trophic levels (i.e., natural enemies). Here, we investigated the effects of plant sex on herbivore abundance and that of their natural enemies associated with the dioecious shrub Buddleja cordata Kunth (Scrophulariaceae). Furthermore, we measured a subset of plant traits frequently involved in herbivore resistance and the potentially underlying plant sex effects. To this end, we recorded the abundances of a specialist leaf‐chewing caterpillar [Acronyctodes mexicanaria Walker (Lepidoptera: Geometridae)] throughout an entire growing season. We also recorded information about the caterpillar’s parasitoids, as well as leaf water content, phenolic compounds, phosphorus, and nitrogen for male and female plants of B. cordata. Plant sex did not significantly influence caterpillar abundance but did have an effect on natural enemies, with parasitoid abundance being 2.4‐fold greater on female than on male plants. The effect of plant sex on parasitoids remained significant after accounting for caterpillar abundance, suggesting that it was underlain by a trait‐mediated (rather than density‐mediated) mechanism. Finally, we found that male plants had a higher concentration of phenolic compounds (other traits did not differ between plant sexes). These results provide valuable evidence for the extended effects of plant sex on the third trophic level and point at plant traits potentially mediating such effects.     

Resistance to oxidative stress shows low heritability and high common environmental variance in a wild bird

Oxidative stress was recently demonstrated to affect several fitness‐related traits and is now well recognized to shape animal life‐history evolution. However, very little is known about how much resistance to oxidative stress is determined by genetic and environmental effects and hence about its potential for evolution, especially in wild populations. In addition, our knowledge of phenotypic sexual dimorphism and cross‐sex genetic correlations in resistance to oxidative stress remains extremely limited despite important evolutionary implications. In free‐living great tits (Parus major), we quantified heritability, common environmental effect, sexual dimorphism and cross‐sex genetic correlation in offspring resistance to oxidative stress by performing a split‐nest cross‐fostering experiment where 155 broods were split, and all siblings (n = 791) translocated and raised in two other nests. Resistance to oxidative stress was measured as both oxidative damage to lipids and erythrocyte resistance to a controlled free‐radical attack. Both measurements of oxidative stress showed low additive genetic variances, high common environmental effects and phenotypic sexual dimorphism with males showing a higher resistance to oxidative stress. Cross‐sex genetic correlations were not different from unity, and we found no substantial heritability in resistance to oxidative stress at adult age measured on 39 individuals that recruited the subsequent year. Our study shows that individual ability to resist to oxidative stress is primarily influenced by the common environment and has a low heritability with a consequent low potential for evolution, at least at an early stage of life.