J.EVOL.BIOL.

Many organisms modify their physiological functions by acclimating to changes in their environment. Recent studies of thermal physiology have been influenced by verbal models that fail to consider the selective advantage of acclimation and thus make no predictions about variation in acclimation capacity. We used a quantitative model of optimal plasticity to generate predictions about the capacity of Drosophila melanogaster to acclimate to developmental temperature. This model predicts that the ability to acclimate thermal sensitivity should evolve when temperature varies greatly among generations. Based on the model, we expected that flies from the highly seasonal environment of New Jersey would acclimate thermal sensitivity more than would flies from the less seasonal environment of Florida. When raised at constant and fluctuating temperatures, flies from these populations failed to adjust their thermal optima in the way predicted by the model, suggesting that current assumptions about functional and genetic constraints should be reconsidered.

Inbreeding adversely affects life history traits as well as various other fitness-related traits, but its effect on cognitive traits remains largely unexplored, despite their importance to fitness of many animals under natural conditions. We studied the effects of inbreeding on aversive learning (avoidance of an odour previously associated with mechanical shock) in multiple inbred lines of Drosophila melanogaster derived from a natural population through up to 12 generations of sib mating. Whereas the strongly inbred lines after 12 generations of inbreeding (0.75 < F < 0.93) consistently showed reduced egg-to-adult viability (on average by 28%), the reduction in learning performance varied among assays (average = 18% reduction), being most pronounced for intermediate conditioning intensity. Furthermore, moderately inbred lines (F = 0.38) showed no detectable decline in learning performance, but still had reduced egg-to-adult viability, which indicates that overall inbreeding effects on learning are mild. Learning performance varied among strongly inbred lines, indicating the presence of segregating variance for learning in the base population. However, the learning performance of some inbred lines matched that of outbred flies, supporting the dominance rather than the overdominance model of inbreeding depression for this trait. Across the inbred lines, learning performance was positively correlated with the egg-to-adult viability. This positive genetic correlation contradicts a trade-off observed in previous selection experiments and suggests that much of the genetic variation for learning is owing to pleiotropic effects of genes affecting functions related to survival. These results suggest that genetic variation that affects learning specifically (rather than pleiotropically through general physiological condition) is either low or mostly due to alleles with additive (semi-dominant) effects.

In a metapopulation, the process of recurrent local extinction and recolonization gives rise to an age structure among demes. Recently established demes will tend to differ from older demes in terms of the levels of genetic diversity found within them and the way this diversity is distributed among demes in the same and different ages. The effects of population turnover on average levels of genetic diversity among demes in a metapopulation have been the focus of much attention, both for neutral and nonneutral loci, but much less is known about the distribution of nonneutral genetic diversity among demes of different ages. In this paper, we used computer simulations to study the distribution of genetic load, inbreeding depression and heterosis in an age-structured metapopulation. We found that, for mildly deleterious mutations, within-deme inbreeding depression increased, whereas heterosis and genetic load decreased with deme age following severe colonization bottlenecks. In contrast, recessive lethal alleles tended to be purged during colonization, with older populations showing higher genetic load and higher within-deme inbreeding depression. Heterosis caused by recessive lethal alleles and resulting from gene flow among different demes tended to be greatest for young demes, because the mutations responsible tended to be purged in the first few generations after colonization, but its effects increased again as populations grow older as a result of immigration. Our results point to a need for estimates of genetic diversity, genetic load, within-deme inbreeding depression and heterosis in demes of different age classes separately.

Studies of the attractiveness of female bodies have focussed strongly on the waist, hips and bust, but sexual selection operates on whole phenotypes rather than the relative proportions of just two or three body parts. Here, we use body scanners to extract computer-generated images of 96 Chinese women’s bodies with all traits unrelated to body shape removed. We first show that Chinese and Australian men and women rate the attractiveness of these bodies the same. We then statistically explore the roles of age, body weight and a range of length and girth measures on ratings of attractiveness. Last, we use nonlinear selection analysis, a statistical approach developed by evolutionary biologists to explore the interacting effects of suites of traits on fitness, to study how body traits interact to determine attractiveness. Established proxies of adiposity and reproductive value, including age, body mass index and waist-to-hip ratio, were all correlated with attractiveness. Nonlinear response surface methods using the original traits consistently outperform all of these indices and ratios, suggesting that indices of youth and abdominal adiposity tell only part of the story of body attractiveness. In particular, our findings draw attention to the importance of integration between abdominal measures, including the bust, and the length and girth of limbs. Our results provide the most comprehensive analysis to date of the effect of body shape and fat deposition on female attractiveness.

Sex-dependent selection can help maintain sexual dimorphism. When the magnitude of selection exerted on a heritable sex trait differs between the sexes, it may prevent each sex to reach its phenotypic optimum. As a consequence, the benefit of expressing a sex trait to a given value may differ between males and females favouring sex-specific adaptations associated with different values of a sex trait. The level of metabolites regulated by genes that are under sex-dependent selection may therefore covary with the degree of ornamentation differently in the two sexes. We investigated this prediction in the barn owl, a species in which females display on average larger black spots on the plumage than males, a heritable ornament. This melanin-based colour trait is strongly selected in females and weakly counter-selected in males indicating sex-dependent selection. In nestling barn owls, we found that daily variation in baseline corticosterone levels, a key hormone that mediates life history trade-offs, covaries with spot diameter displayed by their biological parents. When their mother displayed larger spots, nestlings had lower corticosterone levels in the morning and higher levels in the evening, whereas the opposite pattern was found with the size of paternal spots. Our study suggests a link between daily regulation of glucocorticoids and sex-dependent selection exerted on sexually dimorphic melanin-based ornaments.

Recent studies have shown that symbionts can be a source of adaptive phenotypic variation for their hosts. It is assumed that co-evolution between hosts and symbionts underlies these ecologically significant phenotypic traits. We tested this assumption in the ectosymbiotic fungal associate of the gall midge Asteromyia carbonifera. Phylogenetic analysis placed the fungal symbiont within a monophyletic clade formed by Botryosphaeria dothidea, a typically free-living (i.e. not associated with an insect host) plant pathogen. Symbiont isolates from four divergent midge lineages demonstrated none of the patterns common to heritable microbial symbioses, including parallel diversification with their hosts, substitution rate acceleration, or A+T nucleotide bias. Amplified fragment length polymorphism genotyping of the symbiont revealed that within-lineage genetic diversity was not clustered along host population lines. Culture-based experiments demonstrated that the symbiont-mediated variation in gall phenotype is not borne out in the absence of the midge. This study shows that symbionts can be important players in phenotypic variation for their hosts, even in the absence of a co-evolutionary association.

The locomotion of early tetrapods has long been a subject of great interest in the evolutionary history of vertebrates. However, we still do not have a precise understanding of the evolutionary radiation of their locomotory strategies. We present here the first palaeohistological study based on theoretical biomechanical considerations among a highly diversified group of early tetrapods, the temnospondyls. Based on the quantification of microanatomical and histological parameters in the humerus and femur of nine genera, this multivariate analysis provides new insights concerning the adaptations of temnospondyls to their palaeoenvironments during the Early Permian, and clearly after the Permo-Triassic crisis. This study therefore presents a methodology that, if based on a bigger sample, could contribute towards a characterization of the behaviour of species during great evolutionary events.

The steps by which neutral, random and/or negative biological interactions evolve into mutualistic ones remain poorly understood. Here, we study Elacatinus gobies and the ‘client’ fishes they clean. Colourful stripes are common to mutualist cleaners and noncleaning sister species. Blue stripes are unique to cleaners and are more conspicuous to predators than are basal yellow or green stripes. In turn, we focused on the role of colour as a potentially specialized signal. We show that cleaners may possess a chemical defence and demonstrate that stripes are sufficient to elicit client posing behaviour and to deter attack, corroborating the putative role of chemistry. Analysis of previously published records shows that yellow cleaners interact with predatory clients less often compared to green and blue cleaners. Our results highlight evolution from predator resistance to advertising with conspicuous signals. Similar trajectories, via recognizable signals to risky partners, may be common in other diffuse mutualisms.

The evolution of mutualisms under novel selective pressures will play a key role in ecosystem responses to environmental change. Because fixed nitrogen is traded in plant–rhizobium mutualisms, increasing N availability in the soil is predicted to alter coevolution of these interactions. Legumes typically decrease the number of associations (nodules) with rhizobia in response to nitrate, but the evolutionary dynamics of this response remain unknown. We grew plant and rhizobium genotype combinations in three N environments to assess the coevolutionary potential of the nodule nitrate response in natural communities of plants and rhizobia. We found evidence for coevolutionary genetic variation for nodulation in response to nitrate (G × G × E interaction), suggesting that the mutualism response to N deposition will depend on the combination of partner genotypes. Thus, the nitrate response is not a fixed mechanism in plant–rhizobium symbioses, but instead is potentially subject to natural selection and dynamic coevolution.

A trade-off between immune system and moulting is predicted in birds, given that both functions compete for resources. However, it is unclear whether such a trade-off exists during post-breeding moult. This study tests such a trade-off in the house sparrow (Passer domesticus). Males injected with an antigen (lipopolysaccharide) significantly moulted slower than sham-injected males. Moreover, males whose seventh primaries were plucked to simulate moult showed smaller immune response to phytohaemagglutinin than control males, in which seventh primaries were clipped. A trade-off between moult speed and body mass was also found. The results show a clear trade-off between moult and immune response in the house sparrow: immune response negatively affected moult and moult negatively affected immune response. These findings suggest that only individuals in good condition may have an efficient moult and simultaneously respond effectively in terms of immunity to pathogens, which could explain how plumage traits honestly indicate parasite resistance in birds.

Males and females of dioecious plants often differ in morphological, physiological and life-history traits, probably as a result of their different requirements for reproduction. We found that the growth and reproductive effort of individuals of the dioecious herb Mercurialis annua depended on whether males or females had been growing in the soil previously. This suggests that males and females of M. annua differentially modify the soil in which they are growing. Our study indicates that sexual dimorphism in dioecious plants can give rise to increased environmental heterogeneity as a consequence of sex-specific niche modification.

Recently, two squirrel species (Spermophilus spp.) were discovered to anoint their bodies with rattlesnake scent as a means of concealing their odour from these chemosensory predators. In this study, we tested multiple species with predator scents (rattlesnake and weasel) to determine the prevalence of scent application across the squirrel phylogeny. We reconstructed the evolutionary history of the behaviour using a phylogenetic analysis and fossil records of historic predator co-occurrence. Squirrels with historical and current rattlesnake co-occurrence all applied rattlesnake scent, whereas no relationship existed between weasel scent application and either weasel or rattlesnake co-occurrence. This was surprising because experimental tests confirmed rattlesnake and weasel scent were both effective at masking prey odour from hunting rattlesnakes (the primary predator of squirrels). Ancestral reconstructions and fossil data suggest predator scent application in squirrels is ancient in origin, arising before co-occurrences with rattlesnakes or weasels in response to some other, now extinct, chemosensory predator.

The metabolic distinction between endotherms and ectotherms is profound. Whereas the ecology of metabolic rates is well studied, how endotherms evolved from their ectothermic ancestors remains unclear. The aerobic capacity model postulates that a genetic constraint between resting and maximal metabolism was essential for the evolution of endothermy. Using the multivariate breeders’ equation, I illustrate how the (i) relative sizes of genetic variances and (ii) relative magnitudes of selection gradients for resting and maximal metabolism affect the genetic correlation needed for endothermy to have evolved via a correlated response to selection. If genetic variances in existing populations are representative of ancestral conditions, then the aerobic capacity model is viable even if the genetic correlation was modest. The analyses reveal how contemporary data on selection and genetic architecture can be used to test hypotheses about the evolution of endothermy, and they show the benefits of explicitly linking physiology and quantitative genetic theory.

Genome scans have been used in the studies of ecological speciation to find genomic regions (‘outlier loci’) showing reduced gene flow between divergent populations/species. High-throughput sequencing (‘454’) offers new opportunities in this field via transcriptome sequencing. Divergent ecotypes of the marine gastropod Littorina saxatilis represent a good example of incipient ecological speciation. We performed a 454-based genome scan between H and M ecotypes of L. saxatilis from the British Isles using cDNA of pooled individuals. Allele frequencies were calculated for 2454 single nucleotide polymorphisms (SNPs), within 572 contigs, and 7% of loci were detected as outliers. Functional annotation of the contigs containing outlier SNPs showed that they included shell matrix and muscle proteins (lithostathine, mucin, titin), proteins involved in energetic metabolism (arginine kinase, NADH dehydrogenase) and reverse transcriptases. Follow-up investigations into these proteins and unannotated outliers will be a promising route in the study of ecological speciation in L. saxatilis.

The Pleistocene to Holocene transition was accompanied by a worldwide extinction event affecting numerous mammalian species. Several species such as the woolly mammoth and the giant deer survived this extinction wave, only to go extinct a few thousand years later during the Holocene. Another example for such a Holocene extinction is the Don-hare, Lepus tanaiticus, which inhabited the Russian plains during the late glacial. After being slowly replaced by the extant mountain hare (Lepus timidus), it eventually went extinct during the middle Holocene. Here, we report the phylogenetic relationship of L. tanaiticus and L. timidus based on a 339-basepair (bp) fragment of the mitochondrial D-loop. Phylogenetic tree- and network reconstructions do not support L. tanaiticus and L. timidus being different species. Rather, we suggest that the two taxa represent different morphotypes of a single species and the extinction of ‘L. tanaiticus’ represents the disappearance of a local morphotype rather than the extinction of a species.

Geographical variation in traits related to fitness is often the result of adaptive evolution. Stress resistance traits in Drosophila often show clinal variation, suggesting that selection affects resistance traits either directly or indirectly. Multiple stress resistance traits were investigated in 45 natural populations of Drosophila ananassae collected from all over India. There was significant positive correlation between starvation resistance and lipid content. Significant negative correlations between desiccation and lipid content and between desiccation and heat resistance were also found. Flies from lower latitudes had higher starvation resistance, heat resistance and lipid content but the pattern was reversed for desiccation resistance. These results suggest that flies from different localities varied in their susceptibility to starvation because of difference in their propensity to store body lipid. Multiple regression analysis provided evidence of climatic selection driven by latitudinal variation in the seasonal amplitude of temperature and humidity changes within the Indian. Finally, our results suggest a high degree of variation in stress resistance at the population level in D. ananassae.

Selection for different fitness optima between sexes is supposed to operate on several traits. As fitness-related traits are often energetically costly, selection should also act directly on the energetics of individuals. However, efforts to examine the relationship between fitness and components of the energy budget are surprisingly scarce. We investigated the effects of basal metabolic rate (BMR, the minimum energy required for basic life functions) and body condition on long-term survival (8 winter months) with manipulated densities in enclosed populations of bank voles (Myodes glareolus). Here, we show that survival selection on BMR was clearly sex-specific but density-independent. Both the linear selection gradient and selection differential for BMR were positive in females, whereas survival did not correlate with male characteristics. Our findings emphasize the relative importance of individual physiology over ecological factors (e.g. intra-specific competition). Most current models of the origin of endothermy underline the importance of metabolic optima in females, whose physiology evolved to fulfil demands of parental provisioning in mammals. Our novel findings of sex-specific selection could be related to these life history differences between sexes.

Using Drosophila melanogaster, we explore the consequences of restricted panmixia (RP) on the genetic load caused by segregating deleterious recessive alleles in a population where females mate a full sib with probability about ½ and mate randomly otherwise. We find that this breeding structure purges roughly half the load concealed in heterozygous condition. Furthermore, fitness did not increase after panmixia was restored, implying that, during RP, the excess of expressed load induced by inbreeding had also been efficiently purged. We find evidences for adaptation to laboratory conditions and to specific selective pressures imposed by the RP protocol. We discuss some of the consequences of these results, both for the evolution of population breeding structures and for the design of conservation programmes.

The evolutionary forces shaping within- and across-species variation in the investment in male and female sex function are still incompletely understood. Despite earlier suggestions that in plants the evolution or cosexuality vs. dioecy, as well as sex allocation among cosexuals, is affected by seed and pollen dispersal, no formal model has explicitly used dispersal distances to address this problem. Here, we present a game-theory model as well as a simulation study that fills in this gap. Our model predicts that dioecy should evolve if seeds and pollen disperse widely and that sex allocation among cosexuals should be biased towards whichever sex function produces more widely dispersing units. Dispersal limitations stabilize cosexuality by reinforcing competition between spatially clumped dispersal units from the same source, leading to saturating fitness returns that render sexual specialization unprofitable. However, limited pollen dispersal can also increase the risk of selfing, thus potentially selecting for dioecy as an outbreeding mechanism. Finally, we refute a recent claim that cosexuals should always invest equally in both sex functions.

Sensory drive, where the efficacy of a sexual signal depends on the environment in which it is employed, is a potential mechanism behind divergent evolution of secondary sexual traits. Male swordtail characins are equipped with a narrow and transparent extension of the gill cover with a flag-like structure at its tip. This opercular flag mimics a prey item and is employed by males as a ‘lure’ to attract the attention of females during mating attempts. We conducted a study of genetic and morphological differentiation across swordtail characin populations throughout their native range in Trinidad. The morphology of the opercular flag varied across populations and several aspects of this variation match the predicted hallmarks of sensory drive. First, morphological differentiation of the flag across populations was unrelated to genetic similarity at neutral genetic markers. Second, the shape of the flag covaried with those aspects of body shape that should reflect adaptation to different feeding regimes. Third, and most importantly, the shape of the flag covaried across populations with those environmental characteristics that should most closely reflect differences in local prey abundance. Overall, our results are consistent with a scenario where the evolution of this male sexual signal tracks food-related shifts in female sensory biases across populations, thus providing at least provisional support for a role for sensory drive in population differentiation.