When environmental variation is spatially continuous, dispersing individuals move among nearby sites with similar habitat conditions. But as an environmental gradient becomes steeper, gene flow may connect more divergent habitats, and this is predicted to reduce the slope of the adaptive dine that evolves. We compared quantitative genetic divergence of Rana temporaria frog populations along a 2,000-m elevational gradient in eastern Switzerland (new experimental results) with divergence along a 1,550-km latitudinal gradient in Fennoscandia (previously published results). Both studies found significant countergradient variation in larval development rate (i.e., animals from cold climates developed more rapidly). The dine was weaker with elevation than with latitude. Animals collected on both gradients were genotyped at similar to 2,000 singlenucleotide polymorphism markers, revealing that dispersal distance was 30% farther on the latitudinal gradient but 3.9 times greater with respect to environmental conditions on the elevational gradient. A meta-analysis of 19 experimental studies of anuran populations spanning temperature gradients revealed that countergradient variation in larval development, while significant overal I, was weaker when measured on steeper gradients. These findings support the prediction that adaptive population divergence is less pronounced, and maladaptation more pervasive, on steep environmental gradients.
The evolution of male traits that inflict direct harm on females during mating interactions can result in a so-called tragedy of the commons, where selfish male strategies depress population viability. This tragedy of the commons can be magnified by intralocus sexual conflict (IaSC) whenever alleles that reduce fecundity when expressed in females spread in the population because of their benefits in males. We evaluated this prediction by detailed phenotyping of 73 isofemale lines of the seed beetle Callosobruchus maculatus. We quantified genetic variation in life history andmorphology, as well as associated covariance in male and female adult reproductive success. In parallel, we created replicated artificial populations of each line and measured their productivity. Genetic constraints limited independent trait expression in the sexes, and we identified several instances of sexually antagonistic covariance between traits and fitness, signifying IaSC. Population productivity was strongly positively correlated to female adult reproductive success but uncorrelated with male reproductive success. Moreover, male (female) phenotypic optima for several traits under sexually antagonistic selection were exhibited by the genotypes with the lowest (highest) population productivity. Our study forms a direct link between individuallevel sex-specific selection and population demography and places lifehistory traits at the epicenter of these dynamics.
Although understanding female reproduction is crucial for population demography, determining how and to what relative extent it is constrained by different ecological factors is complicated by difficulties in studying the links between individual behavior, life history, and fitness in nature. We present data on females in a natural population of the butterfly Leptidea sinapis. These data were combined with climate records and laboratory estimates of life-history parameters to predict the relative impact of different ecological constraints on female fitness in the wild. Using simulation models, we partitioned effects of male courtship, host plant availability, and temperature on female fitness. Results of these models indicate that temperature is the most constraining factor on female fitness, followed by host plant availability; the short-term negative effects of male courtship that were detected in the field study were less important in models predicting female reproductive success over the entire life span. In the simulations, females with more reproductive reserves were more limited by the ecological variables. Reproductive physiology and egg-laying behavior were therefore predicted to be co-optimized but reach different optima for females of different body sizes; this prediction is supported by the empirical data. This study thus highlights the need for studying behavioral and life-history variation in orchestration to achieve a more complete picture of both demographic and evolutionary processes in naturally variable and unpredictable environments.
We investigate whether males limit the reproductive success of females in the two pipefish species Syngnathus typhle and Nerophis ophidion. Syngnathus typhle is sexually monomorphic, and courtship behavior does not differ between the sexes. In N. ophidion, on the contrary, females are larger, more colorful, and more active during courtship, possessing appearance-enlarging skin folds. In both species, males brood the offspring on their bodies, one internally and one externally. Males do not invest more energy in reproduction than do females, and in the sexually dimorphic species, males invest even less than females do. Natural sex ratios are equal in both species. Experimentally, we provided each female with an excess of males (i.e., three), in order to measure a female's maximal reproductive rate, and found that females of both species produced more eggs, or produced them at a faster rate, than naturally available males could care for. Within the time span of one male pregnancy, S. typhle females filled an average of 1.9 males and N. ophidion an average of 1.8 males; both numbers are significantly more than one (which is the average mate availability in natural populations). Measured in another way, during one male pregnancy, S. typhle and N. ophidion females both produced 41% more eggs than needed to fill a male, significantly more than no egg surplus in both species. Therefore, brood space and the rate of embryonic development limit female reproduction in these species. There was no significant difference between the species, however. Syngnathus typhle males might be expected to be less limiting than N. ophidion males, but sexual size dimorphism may be absent in S. typhle because, by contrast with N. ophidion, larger males enjoy greater reproductive success. Directional selection for increased male size may decrease sexual size dimorphism in S. typhle. At any rate, the limitation of the reproductive success of one sex by the other seems to be a necessary but not sufficient prerequisite for the evolution of sexual dimorphism and "sex roles."
Extreme F-2 phenotypes known as transgressive segregants can cause increased or decreased fitness in hybrids beyond the ranges seen in parental populations. Despite the usefulness of transgression for plant and animal breeding and its potential role in hybrid speciation, the genetic mechanisms and predictors of transgressive segregation remain largely untested. We generated seven hybrid crosses between five widely divergent Saccharomyces yeast species and measured the fitness of the parents and their viable F-1 and F-2 hybrids in seven stressful environments. We found that on average 16.6% of all replicate F-2 hybrids had higher fitness than both parents. Against our predictions, transgression frequency was not a function of parental genetic and phenotypic distances across test environments. Within environments, some relationships were significant, but not in the predicted direction; for example, genetic distance was negatively related to transgression in ethanol and hydrogen peroxide. Significant effects of hybrid cross, test environment, and cross x environment interactions suggest that the amount of transgression produced in a hybrid cross is highly context specific and that outcomes of hybridization differ even among crosses made from the same two parents. If the goal is to reliably predict hybrid fitness and forecast the evolutionary potential of admixed populations, we need more efforts to identify patterns beyond the idiosyncrasies caused by specific genomic or environmental contexts.
Senescence is the decline in survival and reproduction as an organism ages and is known to occur in collared flycatchers Ficedula albicollis. We consider annual fitness (the estimated genetic contribution that an individual makes to next year’s gene pool) as a measure of age‐specific fitness. We apply a restricted maximum likelihood linear mixed‐model approach on 25 years of data on 3,844 male and 4,992 female collared flycatchers. Annual fitness had a significant additive genetic component (h2 of about 4%). Annual fitness declined at later ages in both sexes. Using a random regression animal model, we show that the observed age‐related phenotypic changes in annual fitness were not present on the additive genetic level, contrary to predictions of genetic hypotheses of senescence. Our study suggests that patterns of aging in the wild need to be interpreted with caution in terms of underlying genetics because they may be largely determined by environmental processes.
In many socially monogamous animals, females engage in extrapair copulation (EPC), causing some broods to contain both within-pair and extrapair young (EPY). The proportion of all young that are EPY varies across populations and species. Because an EPC that does not result in EPY leaves no forensic trace, this variation in the proportion of EPY reflects both variation in the tendency to engage in EPC and variation in the extrapair fertilization (EPF) process across populations and species. We analyzed data on the distribution of EPY in broods of four passerines (blue tit, great tit, collared flycatcher, and pied flycatcher), with 18,564 genotyped nestlings from 2,346 broods in two to nine populations per species. Our Bayesian modeling approach estimated the underlying probability function of EPC (assumed to be a Poisson function) and conditional binomial EPF probability. We used an information theoretical approach to show that the expected distribution of EPC per female varies across populations but that EPF probabilities vary on the above-species level (tits vs. flycatchers). Hence, for these four passerines, our model suggests that the probability of an EPC mainly is determined by ecological (population-specific) conditions, whereas EPF probabilities reflect processes that are fixed above the species level.
Although many selection estimates have been published, the environmental factors that cause selection to vary in space and time have rarely been identified. One way to identify these factors is by experimentally manipulating the environment and measuring selection in each treatment. We compiled and analyzed selection estimates from experimental studies. First, we tested whether the effect of manipulating the environment on selection gradients depends on taxon, trait type, or fitness component. We found that the effect of manipulating the environment was larger when selection was measured on life-history traits or via survival. Second, we tested two predictions about the environmental factors that cause variation in selection. We found support for the prediction that variation in selection is more likely to be caused by environmental factors that have a large effect on mean fitness but not for the prediction that variation is more likely to be caused by biotic factors. Third, we compared selection gradients from experimental and observational studies. We found that selection varied more among treatments in experimental studies than among spatial and temporal replicates in observational studies, suggesting that experimental studies can detect relationships between environmental factors and selection that would not be apparent in observational studies.
Microbes produce many molecules that are important for their growth and development, and the exploitation of these secretions by nonproducers has recently become an important paradigm in microbial social evolution. Although the production of these public-goods molecules has been studied intensely, little is known of how the benefits accrued and the costs incurred depend on the quantity of public-goods molecules produced. We focus here on the relationship between the shape of the benefit curve and cellular density, using a model assuming three types of benefit functions: diminishing, accelerating, and sigmoidal (accelerating and then diminishing). We classify the latter two as being synergistic and argue that sigmoidal curves are common in microbial systems. Synergistic benefit curves interact with group sizes to give very different expected evolutionary dynamics. In particular, we show that whether and to what extent microbes evolve to produce public goods depends strongly on group size. We show that synergy can create an "evolutionary trap" that can stymie the establishment and maintenance of cooperation. By allowing density-dependent regulation of production (quorum sensing), we show how this trap may be avoided. We discuss the implications of our results on experimental design.
The way females utilize the gametes of different males has important consequences for sexual selection, sexual conflict, and intersexual coevolution in natural populations. However, patterns of sperm utilization by females are difficult to demonstrate, and their functional significance remains unclear. Here, we experimentally study sperm ejection in the fowl Gallus gallus domesticus, where females eject preferentially the sperm of socially subordinate males. We study two measures of sperm ejection, (i) the probability that an ejaculate is ejected ("risk") and (ii) the proportion of semen ejected ("intensity"), and show that both measures are strongly non-random with respect to characteristics of the ejaculate, the male, and the female. Sperm ejection neutralized on average 80% of an ejaculate, and while larger ejaculates suffered a higher ejection risk, smaller ejaculates suffered more intense ejection. After controlling for ejaculate volume, we found socially subdominant males suffered higher ejection intensity. After controlling for male and ejaculate effects, we found ejection risk increased and intensity declined as females mated with successive males. Collectively, these results reveal that sperm ejection risk and intensity are at least partly actively caused by female behavior and generate independent selective pressures on male and ejaculate phenotypes.
A key assumption of the ideal free distribution (IFD) is that there are no costs in moving between habitat patches. However, because many populations exhibit more or less continuous population movement between patches and traveling cost is a frequent factor, it is important to determine the effects of costs on expected population movement patterns and spatial distributions. We consider a food chain (tritrophic or bitrophic) in which one species moves between patches, with energy cost or mortality risk in movement. In the two-patch case, assuming forced movement in one direction, an evolutionarily stable strategy requires bidirectional movement, even if costs during movement are high. In the N-patch case, assuming that at least one patch is linked bidirectionally to all other patches, optimal movement rates can lead to source-sink dynamics where patches with negative growth rates are maintained by other patches with positive growth rates. As well, dispersal between patches is not balanced (even in the two-patch case), leading to a deviation from the IFD. Our results indicate that cost-associated forced movement can have important consequences for spatial metapopulation dynamics. Relevance to marine reserve design and the study of stream communities subject to drift is discussed.
Recent studies have uncovered an abundance of non-neutral cytoplasmic genetic variation within species, which suggests that we should no longer consider the cytoplasm an idle intermediary of evolutionary change. Nonneutrality of cytoplasmic genomes is particularly intriguing, given that these genomes are maternally transmitted. This means that the fate of any given cytoplasmic genetic mutation is directly tied to its performance when expressed in females. For this reason, it has been hypothesized that cytoplasmic genes will coevolve via a sexually antagonistic arms race with the biparentally transmitted nuclear genes with which they interact. We assess this prediction, examining the intergenomic contributions to the costs and benefits of mating in Callosobruchus maculatus females subjected to a mating treatment with three classes (kept virgin, mated once, or forced to cohabit with a male). We find no evidence that the economics of mating are determined by interactions between cytoplasmic genes expressed in females and nuclear genes expressed in males and, therefore, no support for a sexually antagonistic intergenomic arms race. The cost of mating to females was, however, shaped by an interaction between the cytoplasmic and nuclear genes expressed within females. Thus, cytonuclear interactions are embroiled in the economics of mating.
Predators can cause a shift in both density and frequency of a prey phenotype that may lead to phenotypic divergence through natural selection. What is less investigated is that predators have a variety of indirect effects on prey that could potentially have large evolutionary responses. We conducted a pond experiment to test whether differences in predation risk in different habitats caused shifts in behavior of prey that, in turn, would affect their morphology. We also tested whether the experimental data could explain the morphological variation of perch in the natural environment. In the experiment, predators caused the prey fish to shift to the habitat with the lower predation risk. The prey specialized on habitat-specific resources, and there was a strong correlation between diet of the prey fish and morphological variation, suggesting that resource specialization ultimately affected the morphology. The lack of differences in competition and mortality suggest that the morphological variation among prey was induced by differences in predation risk among habitats. The field study demonstrated that there are differences in growth related to morphology of perch in two different habitats. Thus, a trade-off between foraging and predator avoidance could be responsible for adaptive morphological variation of young perch.
Carotenoid-based coloration plays an important role in signaling, is often sexually dimorphic, and is potentially subject to directional and/or sex-specific selection. To understand the evolutionary dynamics of such color traits, it is essential to quantify patterns of inheritance, yet nonautosomal sources of genetic variation are easily overlooked by classical heritability analyses. Carotenoid metabolism has recently been linked to mitochondria, highlighting the potential for color variation to be explained by cytoplasmically inherited factors. In this study, we used quantitative genetic animal models to estimate the importance of mitochondrial and sex chromosome-linked sources of genetic variation in coloration in two songbird populations in which dietary carotenoids are either unmodified (great tit plumage) or metabolized into alternative color forms (zebra finch beak). We found no significant Z-linked genetic variance in great tit plumage coloration, while zebra finch beak coloration exhibited significant W linkage and cytoplasmic inheritance. Our results support cytoplasmic inheritance of color in the zebra finch, a trait based on endogenously metabolized carotenoids, and demonstrate the potential for nonautosomal sources to account for a considerable share of genetic variation in coloration. Although often overlooked, such nonautosomal genetic variation exhibits sex-dependent patterns of inheritance and potentially influences the evolution of sexual dichromatism.
The information content of signals such as animal coloration depends on the extent to which variation reflects underlying biological processes. Although animal coloration has received considerable attention, little work has addressed the quantitative genetics of color variation in natural populations. We investigated the quantitative genetics of a carotenoid-based color patch, the ventral plumage of mature great tits (Parus major), in a wild population. Carotenoid-based colors are often suggested to reflect environmental variation in carotenoid availability, but numerous mechanisms could also lead to genetic variation in coloration. Analyses of individuals of known origin showed that, although plumage chromaticity (i.e., color) was moderately heritable, there was no significant heritability to achromaticity (i.e., brightness). We detected multiple long-lasting effects of natal environment, with hatching date and brood size both negatively related to plumage chromaticity at maturity. Our reflectance measures contrasted in their spatiotemporal sensitivity, with plumage chromaticity exhibiting significant spatial variation and achromatic variation exhibiting marked annual variation. Hence, color variation in this species reflects both genetic and environmental influences on different scales. Our analyses demonstrate the context dependence of components of color variation and suggest that color patches may convey multiple aspects of individual state.
A positive relationship between occupancy and average local abundance of species is found in a variety of taxa, yet the mechanisms driving this association between abundance and occupancy are still enigmatic. Here we show that freshwater fishes exhibit a positive abundance-occupancy relationship across 125 Swedish lakes. For a subset of 9 species from 11 lakes, we estimated species-specific diet breadth from stable isotopes, within-lake habitat breadth from catch data for littoral and pelagic nets, adaptive potential from genetic diversity, abiotic niche position, and dispersal capacity. Average local abundance was mainly positively associated with both within-lake habitat and diet breadth, that is, species with larger intraspecific variation in niche space had higher abundances. No measure was a good predictor of occupancy, indicating that occupancy may be more directly related to abundance or abiotic conditions than to niche breadth per se. This study suggests a link between intraspecific niche variation and a positive abundance-occupancy relationship and implies that management of freshwater fish communities, whether to conserve threatened or control invasive species, should initially be aimed at niche processes.
The relative roles of evolutionary history and geographical and ecological contingency for community assembly remain unknown. Plant species, for instance, share more phytophages with closer relatives (phylogenetic conservatism), but for exotic plants introduced to another continent, this may be overlaid by geographically contingent evolution or immigration from locally abundant plant species (mass effects). We assessed within local forests to what extent exotic trees (Douglas-fir, red oak) recruit phytophages (Coleoptera, Heteroptera) from more closely or more distantly related native plants. We found that exotics shared more phytophages with natives from the same major plant lineage (angiosperms vs. gymnosperms) than with natives from the other lineage. This was particularly true for Heteroptera, and it emphasizes the role of host specialization in phylogenetic conservatism of host use. However, for Coleoptera on Douglas-fir, mass effects were important: immigration from beech increased with increasing beech abundance. Within a plant phylum, phylogenetic proximity of exotics and natives increased phytophage similarity, primarily in younger Coleoptera clades on angiosperms, emphasizing a role of past codiversification of hosts and phytophages. Overall, phylogenetic conservatism can shape the assembly of local phytophage communities on exotic trees. Whether it outweighs geographic contingency and mass effects depends on the interplay of phylogenetic scale, local abundance of native tree species, and the biology and evolutionary history of the phytophage taxon.
Siring success of flowering plants depends on the fates of male gametophytes, which compete for access to stigmas, stylar resources, and ovules. Although rarely considered, pollen may often compete during dispersal, affecting the processes required for export to stigmas: pollen pickup, transport, and deposition. We quantified dispersal interference by tracking bee-mediated dispersal of stained Anacamptis morio (Orchidaceae) pollen from individual donor flowers and inferred the affected dispersal mechanisms on the basis of the fit of a process-based model. During individual trials, all recipient flowers were either emasculated, precluding interference with donor pollen, or intact, adding potentially interfering pollen to the pollinator. The presence of competing pollinaria on bees reduced pickup of additional pollinaria, doubled the overall proportion of lost donor pollen, and reduced total pollen export by 27%. Interference specifically increased loss of donor pollen between successive flower visits and variation in deposition among trials, and it likely also reduced pollen contact with stigmas and pollen deposition when contact occurred. Thus, by altering pollen removal, transport, and deposition, male-male interference during pollen dispersal can significantly—and perhaps commonly—limit plant-siring success.
Only during the past decade have vision-system-neutral methods become common practice in studies of animal color signals. Consequently, much of the current knowledge on sexual selection is based directly or indirectly on human vision, which may or may not emphasize spectral information in a signal differently from the intended receiver. In an attempt to quantify this discrepancy, we used retinal models to test whether human and bird vision rank plumage colors similarly. Of 67 species, human and bird models disagreed in 26 as to which pair of patches in the plumage provides the strongest color contrast or which male in a random pair is the more colorful. These results were only partly attributable to human UV blindness. Despite confirming a strong correlation between avian and human color discrimination, we conclude that a significant proportion of the information in avian visual signals may be lost in translation.
The avian incubation period is associated with high energetic costs and mortality risks suggesting that there should be strong selection to reduce the duration to the minimum required for normal offspring development. Although there is much variation in the duration of the incubation period across species, there is also variation within species. It is necessary to estimate to what extent this variation is genetically determined if we want to predict the evolutionary potential of this trait. Here we use a long-term study of collared flycatchers to examine the genetic basis of variation in incubation duration. We demonstrate limited genetic variance as reflected in the low and nonsignificant additive genetic variance, with a corresponding heritability of 0.04 and coefficient of additive genetic variance of 2.16. Any selection acting on incubation duration will therefore be inefficient. To our knowledge, this is the first time heritability of incubation duration has been estimated in a natural bird population.
Bergmann's rule predicts a decrease in body size with increasing temperature and has much empirical support. Surprisingly, we know very little about whether "Bergmann size clines" are due to a genetic response or are a consequence of phenotypic plasticity. Here, we use data on body size (mass and tarsus length) from three long-term (1979-2008) study populations of great tits (Parus major) that experienced a temperature increase to examine mechanisms behind Bergmann's rule. We show that adult body mass decreased over the study period in all populations and that tarsus length increased in one population. Both body mass and tarsus length were heritable and under weak positive directional selection, predicting an increase, rather than a decrease, in body mass. There was no support for microevolutionary change, and thus the observed declines in body mass were likely a result of phenotypic plasticity. Interestingly, this plasticity was not in direct response to temperature changes but seemed to be due to changes in prey dynamics. Our results caution against interpreting recent phenotypic body size declines as adaptive evolutionary responses to temperature changes and highlight the importance of considering alternative environmental factors when testing size clines.
Sexual reproduction in eukaryotes implies a biphasic life cycle with alternating haploid and diploid phases. The nature of the biphasic life cycle varies markedly across taxa, and often either the diploid or the haploid phase is predominant. Why some taxa spend a major part of their life cycle as diploids and others as haploids remains a conundrum. Furthermore, ploidy levels may not only vary across life cycle phases but may also differ between males and females. The existence of two life cycle phases and two sexes bears a high potential for antagonistic selection, which in turn may influence the evolution of ploidy levels. We explored the evolution of ploidy levels when selection depends on both ploidy and sex. Our analyses show that antagonistic selection may drive the ploidy levels between males and females apart. In a subsequent step, we explicitly explored the evolution of arrhenotoky (i.e., haploid males and diploid females) in the context of antagonistic selection. Our model shows that selection on arrhenotoky depends on male fitness but evolves regardless of the fitness consequences to females. Overall we provide a plausible explanation for the evolution of sex differences in ploidy levels, a principle that can be extended to any system with asymmetric inheritance.
Classical models studying the evolution of self-fertilization in plants conclude that only complete selfing and complete outcrossing are evolutionarily stable. In contrast with this prediction, 42% of seed-plant species are reported to have rates of self-fertilization between 0.2 and 0.8. We propose that many previous models fail to predict intermediate selfing rates because they do not allow for functional relationships among three components of reproductive fitness: self-fertilized ovules, outcrossed ovules, and ovules sired by successful pollen export. Because the optimal design for fertility components may differ, conflicts among the alternative pathways to fitness are possible, and the greatest fertility may be achieved with some self-fertilization. Here we develop and analyze a model to predict optimal selfing rates that includes a range of possible relationships among the three components of reproductive fitness, as well as the effects of evolving inbreeding depression caused by deleterious mutations and of selection on total seed number. We demonstrate that intermediate selfing is optimal for a wide variety of relationships among fitness components and that inbreeding depression is not a good predictor of selfing-rate evolution. Functional relationships subsume the myriad effects of individual plant traits and thus offer a more general and simpler perspective on mating system evolution.
Males and females differ with respect to life span and rate of aging in most animal species. Such sexual dimorphism can be associated with a complex genetic architecture, where only part of the genetic variation is shared between the sexes. However, the extent to which this is true for life span and aging is not known, because studies of life span have given contradictory results and aging has not been studied from this perspective. Here we investigate the additive genetic architecture of life span and aging in Drosophila melanogaster. We find substantial amounts of additive genetic variation for both traits, with more than three-quarters of this variation available for sex-specific evolutionary change. This result shows that the sexes have a profoundly different additive genetic basis for these traits, which has several implications. First, it translates into an, on average, three-times-higher heritability of life span within, compared to between, the sexes. Second, it implies that the sexes are relatively free to evolve with respect to these traits. And third, as life span and aging are traits that integrate over all genetic factors that contribute to mortal disease, it also implies that the genetics of heritable disease differs vastly between the sexes.
Many sexually selected traits in male fishes are controlled by testosterone. Directional selection for male ornaments could theoretically increase male testosterone levels over evolutionary time-scales, and when genetically correlated, female testosterone levels as well. Because of the negative fitness consequences of high testosterone, it is plausible that female choice for sexually selected traits in males results in decreased female reproductive fitness. I used comparative analysis to examine the association between male peak testosterone expression and sexually selected ornaments. I also tested for genetic correlation between male and female androgen levels. The presence of sexually selected traits in males was significantly correlated with increased peak androgen levels in males as well as females, and female testosterone levels were significantly correlated with male peak testosterone titers, although the slope was only marginally < 1. This suggests that selection to decouple high male and female testosterone levels is either weak or otherwise ineffective.
The numerous physiological and phenotypic differences between the sexes, as well as the disparity between male and female reproductive interests, result in sexual conflicts, which are often manifested at the genomic level. Sexually antagonistic genes benefit one sex at the expense of the other and experience strong pressure to evolve male- and female-specific expression patterns to resolve sexual conflicts and maximize fitness for both sexes. Sex-biased gene expression has recently been demonstrated for much of the metazoan transcriptome, suggesting that many loci are sexually antagonistic. However, many coding regions function in multiple processes throughout the organism. This pleiotropy increases the complexity of selection for any given gene, which in turn may obscure sex-specific selective pressures and hamper the evolution of sex-biased gene expression. Here we use microarray gene expression data, in conjunction with data on transcript abundance from expressed sequence tag libraries, to demonstrate that loci with sex-biased gene expression are significantly less pleiotropic than unbiased genes. This relationship was independent of sex chromosome gene dosage effects, and the results were concordant across two study organisms, chicken and mouse. These results suggest that the resolution of sexually antagonistic gene expression is determined by the evolutionary constraints acting on any given antagonistic locus.
Predicting the impact of climate change on biodiversity requires understanding the adaptation potential of wild organisms. Evolutionary responses depend on the additive genetic variation associated with the phenotypic traits targeted by selection. We combine 5 years of cross-fostering experiments, measurements of resting metabolic rate (RMR) on nearly 200 wild collared flycatcher (Ficedula albicollis) nestlings, and animal models using a 17-year pedigree to evaluate the potential for an evolutionary response to changing environmental conditions. Contrary to other avian studies, we find no significant heritability of whole-organism, mass-independent, or mass-specific RMR, but we report a strong effect of nest environment instead. We therefore conclude that variation in nestling RMR is explained by variation in the early-life environment provided by the parents. We discuss possible underlying specific parental effects and the importance of taking different mechanisms into account to understand how animals phenotypically adapt (or fail to adapt) to climate change.
The history of life has been driven by evolutionary transitions in individuality, that is, the aggregation of autonomous individuals to form a new, higher-level individual. The fungus Neurospora tetrasperma has recently undergone an evolutionary transition in individuality from homokaryosis (one single type of nuclei in the same cytoplasm) to heterokaryosis (two genetically divergent and free-ranging nuclear types). In this species, selection can act at different levels: while nuclei can compete in their replication and transmission into short-lived asexual spores, at the level of the heterokaryotic individual, cooperation between nuclear types is required to produce the long-lived sexual spores. Conflicts can arise between these two levels of selection if the coevolution between nuclear types is disrupted. Here, we investigated the extent of multilevel selection in three strains of N. tetrasperma. We assessed the ratio between nuclear types under different conditions and measured fitness traits of homo- and heterokaryotic mycelia with varying nuclear ratios. We show that the two nuclei have complementary traits, consistent with division of labor and cooperation. In one strain, for which a recent chromosomal introgression was detected, we observed the occurrence of selfish nuclei, enjoying better replication and transmission than sister nuclei at the same time as being detrimental to the heterokaryon. We hypothesize that introgression has disrupted the coevolution between nuclear types in this strain.
How the ability to acclimate will impact individual performance and ecological interactions under climate change remains poorly understood. Theory predicts that the benefit an organism can gain from acclimating depends on the rate at which temperatures change relative to the time it takes to induce beneficial acclimation. Here, we present a conceptual model showing how slower seasonal changes under climate change can alter species' relative performance when they differ in acclimation rate and magnitude. To test predictions from theory, we performed a microcosm experiment where we reared a mid- and a high-latitude damselfly species alone or together under the rapid seasonality currently experienced at 62 degrees N and the slower seasonality predicted for this latitude under climate change and measured larval growth and survival. To separate acclimation effects from fixed thermal responses, we simulated growth trajectories based on species' growth rates at constant temperatures and quantified how much and how fast species needed to acclimate to match the observed growth trajectories. Consistent with our predictions, the results showed that the midlatitude species had a greater capacity for acclimation than the high-latitude species. Furthermore, since acclimation occurred at a slower rate than seasonal temperature changes, the midlatitude species had a small growth advantage over the high-latitude species under the current seasonality but a greater growth advantage under the slower seasonality predicted for this latitude under climate change. In addition, the two species did not differ in survival under the current seasonality, but the midlatitude species had higher survival under the predicted climate change scenario, possibly because rates of cannibalism were lower when smaller heterospecifics were present. These findings highlight the need to incorporate acclimation rates in ecological models.
Phenotypic plasticity is the ability of one genotype to produce different phenotypes depending on environmental conditions. Several conceptual models emphasize the role of plasticity in promoting reproductive isolation and, ultimately, speciation in populations that forage on two or more resources. These models predict that plasticity plays a critical role in the early stages of speciation, prior to genetic divergence, by facilitating fast phenotypic divergence. The ability to plastically express alternative phenotypes may, however, interfere with the early phase of the formation of reproductive barriers, especially in the absence of geographic barriers. Here, we quantitatively investigate mechanisms under which plasticity can influence progress toward adaptive genetic diversification and ecological speciation. We use a stochastic, individual based model of a predator-prey system incorporating sexual reproduction and mate choice in the predator. Our results show that evolving plasticity promotes the evolution of reproductive isolation under diversifying environments when individuals are able to correctly select a more profitable habitat with respect to their phenotypes (i.e., adaptive habitat choice) and to assortatively mate with relatively similar phenotypes. On the other hand, plasticity facilitates the evolution of plastic generalists when individuals have a limited capacity for adaptive habitat choice. We conclude that plasticity can accelerate the evolution of a reproductive barrier toward adaptive diversification and ecological speciation through enhanced phenotypic differentiation between diverging phenotypes.
When the expectation of future reproduction is reduced by senescence, life-history theory predicts that reproductive effort will increase with increasing age. This idea was examined in the collared flycatcher by estimating whether reproductive costs increase with female age, comparing feeding rates and weight losses of old, "senescent" females (i.e., greater-than-or-equal-to 5 yr old) and middle-aged females (2-3 yr old) with the same breeding phenology and the same brood size, and testing whether feeding rate was correlated with daily energy expenditure and with weight loss of females during the nestling period. There was a negative relationship between fledgling production and subsequent survival among old females (greater-than-or-equal-to 5 yr old), but not among younger age classes, which suggests that reproductive effort increases with age. Also, old females fed their nestlings more often and lost more weight during the nestling period than did middle-aged females. Observed feeding rates were positively correlated with daily energy expenditure and weight loss. Since there was no evidence that individuals that survived to old ages were better at all ages, the results strongly suggest that old collared flycatcher females increase their reproductive effort at the cost of a decreased probability of surviving to the next year. However, the payoff of the increased reproductive effort of old females seemed to be small. We suggest that this is a consequence of a conflict between the sexes over the division of work, because old females generally are mated to younger males that probably have better future prospects. Data on male feeding rates in relation to female feeding rates support this idea.
The frequency and asymmetry of mixed-species mating set the initial stage for the ecological and evolutionary implications of hybridization. How such patterns of mixed-species mating, in turn, are influenced by the combination of mate choice errors and relative species abundance remains largely unknown. We develop a mathematical model that generates predictions for how relative species abundances and mate choice errors affect hybridization patterns. When mate choice errors are small (<5%), the highest frequency of hybridization occurs when one of the hybridizing species is at low abundance, but when mate choice errors are high (>5%), the highest hybridization frequency occurs when species occur in equal proportions. Furthermore, females of the less abundant species are overrepresented in mixed-species matings. We compare our theoretical predictions with empirical data on naturally hybridizing Ficedula flycatchers and find that hybridization is highest when the two species occur in equal abundance, implying rather high mate choice errors. We discuss ecological and evolutionary implications of our findings and encourage future work on hybrid zone dynamics that take demographic aspects, such as relative species abundance, into account.
Adaptive topography is a central concept in evolutionary biology, describing how the mean fitness of a population changes with gene frequencies or mean phenotypes. We use expected population size as a quantity to be maximized by natural selection to show that selection on pairwise combinations of reproductive traits of collared flycatchers caused by fluctuations in population size generated an adaptive topography with distinct peaks often located at intermediate phenotypes. This occurred because r- and K-selection made phenotypes favored at small densities different from those with higher fitness at population sizes close to the carrying capacity K. Fitness decreased rapidly with a delay in the timing of egg laying, with a density-dependent effect especially occurring among early-laying females. The number of fledglings maximizing fitness was larger at small population sizes than when close to K. Finally, there was directional selection for large fledglings independent of population size. We suggest that these patterns can be explained by increased competition for some limiting resources or access to favorable nest sites at high population densities. Thus, r- and K-selection based on expected population size as an evolutionary maximization criterion may influence life-history evolution and constrain the selective responses to changes in the environment.
In patch- or habitat-structured populations, different processes can favor adaptive polymorphism at different scales. While spatial heterogeneity can generate spatially disruptive selection favoring variation between patches, local competition can lead to locally disruptive selection promoting variation within patches. So far, almost all theory has studied these two processes in isolation. Here, we use mathematical modeling to investigate how resource variation within and between habitats influences the evolution of variation in a consumer population where individuals compete in finite patches connected by dispersal. We find that locally and spatially disruptive selection typically act in concert, favoring polymorphism under a wider range of conditions than when in isolation. But when patches are small and dispersal between them is low, kin competition inhibits the emergence of polymorphism, especially when the latter is driven by local competition for resources. We further use our model to clarify what comparisons between trait and neutral genetic differentiation (QST/FST comparisons) can tell about the nature of selection. Overall, our results help us understand the interaction between two major drivers of polymorphism: locally and spatially disruptive selection, and how this interaction is modulated by the unavoidable effects of kin selection under limited dispersal.
The genomic deleterious mutation rate and mean effect are central to the biology and evolution of all species. Large‐statured plants, such as trees, are predicted to have high mutation rates due to mitotic mutation and the absence of a sheltered germ line, but their size and generation time has hindered genetic study. We develop and test approaches for estimating deleterious mutation rates and effects from viability comparisons within the canopy of large‐statured plants. Our methods, inspired by E. J. Klekowski, are a modification of the classic Bateman‐Mukai mutation‐accumulation experiment. Within a canopy, cell lineages accumulate mitotic mutations independently. Gametes or zygotes produced at more distal points by these cell lineages contain more mitotic mutations than those at basal locations, and within‐flower selfs contain more homozygous mutations than between‐flower selfs. The resulting viability differences allow demonstration of lethal mutation with experiments similar in size to assays of genetic load and allow estimates of the rate and effect of new mutations with moderate precision and bias similar to that of classic mutation‐accumulation experiments in small‐statured organisms. These methods open up new possibilities with the potential to provide valuable new insights into the evolutionary genetics of plants.
Seed dispersal shapes ecological and evolutionary dynamics of plant populations. Here, we extend classical diversity measures to study the impact of disperser behavior on seed dispersal. We begin by extending our previous diversity structure approach, which partitioned seed source diversity within and among dispersal sites, into the more general framework of traditional diversity measures. This statistical approach allows an assessment of the extent to which foraging behavior shapes α and γ diversity, as well as the divergence in seed sources among dispersal sites, which we call δ. We also introduce tests to facilitate comparisons of diversity among dispersal sites and seed vectors and to compare overall diversity among sampled systems. We then apply these tools to investigate the diversity blend of parentage resulting from seed dispersal by two avian seed vectors with very different social and foraging behaviors: (1) acorn woodpeckers, transportingQuercus agrifolia acorns, and (2) long-wattled umbrellabirds, transporting Oenocarpus bataua palm nuts. Using these diversity and divergence measures, we test the hypothesis that different foraging behaviors generate distinctive diversity partitions for the two focal tree species. This approach provides a new tool for assessment of the impact of dispersal agents on the seed source structure of plant populations, which can be extended to include the impact of virtually any propagule vector for a range of systems.
Anisogamy has evolved in most sexually reproducing multicellular organisms allowing the definition of the male and female sexes, producing small and large gametes. Anisogamy, as the initial sexual dimorphism, is a good starting point to understand the evolution of further sexual dimorphisms. For instance, it is generally accepted that anisogamy sets the stage for more intense mating competition in males than in females. We argue that this idea stems from a restrictive assumption on the conditions under which anisogamy evolved in the first place: the absence of sperm limitation (assuming that all female gametes are fertilized). Here, we relax this assumption and present a model that considers the coevolution of gamete size with a mating competition trait, starting in a population without dimorphism. We vary gamete density to produce different scenarios of gamete limitation. We show that, while at high gamete density the evolution of anisogamy always results in male investment in competition, gamete limitation at intermediate gamete densities allows for either females or males to invest more into mating competition. Our results thus suggest that anisogamy does not always promote mating competition among males. The conditions under which anisogamy evolves matter, as well as the competition trait.
In many species, males exhibit phenotypic plasticity in sexually selected traits when exposed to social cues about the intensity of sexual competition. To date, however, few studies have tested how this plasticity affects male reproductive success. We initially tested whether male mosquitofish,Gambusia holbrooki(Poeciliidae), change their investment in traits under pre- and postcopulatory sexual selection depending on the social environment. For a full spermatogenesis cycle, focal males were exposed to visual and chemical cues of rivals that were either present (competitive treatment) or absent (control). Males from the competitive treatment had significantly slower-swimming sperm but did not differ in sperm count from control males. When two males competed for a female, competitive treatment males also made significantly fewer copulation attempts and courtship displays than control males. Further, paternity analysis of 708 offspring from 148 potential sires, testing whether these changes in reproductive traits affected male reproductive success, showed that males previously exposed to cues about the presence of rivals sired significantly fewer offspring when competing with a control male. We discuss several possible explanations for these unusual findings.
A high degree of trophic polymorphism has been associated with the absence of high variability in population density. An explanation for this pattern is that density fluctuations may influence selective regime forms in populations. Still, only few studies have investigated evolutionary dynamics in fluctuating populations. Here we report on a multiyear study of the Eurasian perch, wherein the fitness landscape shifts between stabilizing and directional selection at low density to disruptive selection at high density. Intrinsically driven population fluctuations is the mechanism that most likely explains these shifts in fitness landscape. Stable isotope data showed that the habitat choices of perch were stable over the growing season, indicating that the selection pressure observed each year influenced the fitness of perch in the following year’s reproductive period. Furthermore, the morphological differences between perch caught in the two habitats (littoral and pelagic) were more pronounced at high density than at low density. This study shows that an explicit consideration of population dynamics may be essential to explain the long‐term evolutionary dynamics in populations. In particular, fluctuating population dynamics may be one explanation for why not all polymorphic populations lead to speciation. Instead, fluctuating population dynamics may favor the evolution of phenotypic plasticity.
Theoretical and empirical studies are showing evidence in support of evolutionary branching and sympatric speciation due to frequency‐dependent competition. However, phenotypic diversification due to underlying genetic diversification is only one possible evolutionary response to disruptive selection. Another potentially general response is phenotypic diversification in the form of phenotypic plasticity. It has been suggested that genetic variation is favored in stable environments, whereas phenotypic plasticity is favored in unstable and fluctuating environments. We investigate the “competition” between the processes of evolutionary branching and the evolution of phenotypic plasticity in a predator‐prey model that allows both processes to occur. In this model, environmental fluctuations can be caused by complicated population dynamics. We found that the evolution of phenotypic plasticity was generally more likely than evolutionary branching when the ecological dynamics exhibited pronounced predator‐prey cycles, whereas the opposite was true when the ecological dynamics was more stable. At intermediate levels of density cycling, trimorphisms with two specialist branches and a phenotypically plastic generalist branch sometimes occurred. Our theoretical results suggest that ecological dynamics and evolutionary dynamics can often be tightly linked and that an explicit consideration of population dynamics may be essential to explain the evolutionary dynamics of diversification in natural populations.
Phenotypic plasticity may be favored in generalist populations if it increases niche width, even in temporally constant environments. Phenotypic plasticity can increase the frequency of extreme phenotypes in a population and thus allow it to make use of a wide resource spectrum. Here we test the prediction that generalist populations should be more plastic than specialists. In a common-garden experiment, we show that solitary, generalist populations of threespine sticklebacks inhabiting small coastal lakes of British Columbia have a higher degree of morphological plasticity than the more specialized sympatric limnetic and benthic species. The ancestral marine stickleback showed low levels of plasticity similar to those of sympatric sticklebacks, implying that the greater plasticity of the generalist population has evolved recently. Measurements of wild populations show that those with mean trait values intermediate between the benthic and limnetic values indeed have higher morphological variation. Our data indicate that plasticity can evolve rapidly after colonization of a new environment in response to changing niche use.
Rapid evolutionary change over a few generations has been documented in natural populations. Such changes are observed as organisms invade new environments, and they are often triggered by changed interspecific interactions, such as differences in predation regimes. However, in spite of increased recognition of antagonistic male-female mating interactions, there is very limited evidence that such intraspecific interactions could cause rapid evolutionary dynamics in nature. This is because ecological and longitudinal data from natural populations have been lacking. Here we show that in a color-polymorphic damselfly species, male-female mating interactions lead to rapid evolutionary change in morph frequencies between generations. Field data and computer simulations indicate that these changes are driven by sexual conflict, in which morph fecundities are negatively affected by frequency- and density-dependent male mating harassment. These frequency-dependent processes prevent population divergence by maintaining a female polymorphism in most populations. Although these results contrast with the traditional view of how sexual conflict enhances the rate of population divergence, they are consistent with a recent theoretical model of how females may form discrete genetic clusters in response to male mating harassment.
Closely related species often have similar traits and sometimes interact with the same species. A crucial problem in evolutionary ecology is therefore to understand how coevolving species diverge when they interact with a set of closely related species from another lineage rather than with a single species. We evaluated geographic differences in the floral morphology of all woodland star plant species (Lithophragma, Saxifragaceae) that are pollinated by Greya (Prodoxidae) moths. Flowers of each woodland star species differed depending on whether plants interact locally with one, two, or no pollinating moth species. Plants of one species grown in six different environments showed few differences in floral traits, suggesting that the geographic differences are not due significantly to trait plasticity. Greya moth populations also showed significant geographic divergence in morphology, depending on the local host and on whether the moth species co-occurred locally. Divergence in the plants and the moths involved shifts in combinations of partially correlated traits, rather than any one trait. The results indicate that the geographic mosaic of coevolution can be amplified as coevolving lineages diversify into separate species and come together in different combinations in different ecosystems.
Differential reproductive investment by the mother can critically influence offspring development and phenotype, and strong selection is therefore expected to act on such maternal effects. Although a genetic basis is a prerequisite for phenotypic traits to respond to selection and thus to evolve, we still know very little about the extent of heritable variation in maternal effects in natural populations. Here, we present the first estimates of intrafemale repeatability across breeding seasons and estimates of heritability of hormone-mediated maternal effects in a wild population of collared flycatchers (Ficedula albicollis). We found that maternal yolk testosterone (T) concentrations, yolk mass, and egg mass were moderately to highly repeatable within females across years, whereas intrafemale consistency of maternal yolk androstenedione (A4) deposition was low yet statistically significant. Furthermore, maternal yolk T transfer, yolk mass, and egg mass were significantly heritable, whereas yolk A4 transfer was not. These results strongly suggest that two major maternal yolk androgens are differentially regulated by genes and the environment. Selection on heritable variation in maternal yolk T deposition has the potential to shape the rate and direction of phenotypic change in offspring traits and can thereby accelerate or impede the response to selection in natural populations.