Evolution Letters最新文献

Populations are capable of responding to environmental change over ecological timescales via adaptive tracking. However, the translation from patterns of allele frequency change to rapid adaptation of complex traits remains unresolved. We used abdominal pigmentation in Drosophila melanogaster as a model phenotype to address the nature, genetic architecture, and repeatability of rapid adaptation in the field. We show that D. melanogaster pigmentation evolves as a highly parallel and deterministic response to shared environmental variation across latitude and season in natural North American populations. We then experimentally evolved replicate, genetically diverse fly populations in field mesocosms to remove any confounding effects of demography and/or cryptic structure that may drive patterns in wild populations; we show that pigmentation rapidly responds, in parallel, in fewer than 15 generations. Thus, pigmentation evolves concordantly in response to spatial and temporal climatic axes. We next examined whether phenotypic differentiation was associated with allele frequency change at loci with established links to genetic variance in pigmentation in natural populations. We found that across all spatial and temporal scales, phenotypic patterns were associated with variation at pigmentation-related loci, and the sets of genes we identified at each scale were largely nonoverlapping. Therefore, our findings suggest that parallel phenotypic evolution is associated with distinct components of the polygenic architecture shifting across each environmental axis to produce redundant adaptive patterns.

Spatial network structure of biological systems drives ecology and evolution by distributing organisms and their genes. The ubiquitous host-parasite systems are no exception. However, past theoretical work has largely focused on simple spatial structures, such as grids, hampering the translation of theoretical predictions to real ecosystems. Thus, we develop an eco-evolutionary metapopulation model of host-parasite dynamics where hosts and parasites disperse through realistically complex spatial networks representing major biomes using river-like and terrestrial-like networks. We generate the testable prediction that parasite virulence, or how parasites harm their hosts, peaks at intermediate dispersal values in river-like systems while it increases with increasing dispersal in terrestrial-like systems. In river-like systems, virulence also reaches higher overall values. Moreover, we show that kin selection is the main driver of virulence evolution. Spatial networks generate characteristic patterns of parasite relatedness which drive differential virulence evolution. Finally, we show that accounting for virulence evolution allows us to predict the distribution of key epidemiological variables (e.g., parasite extinction risks) within spatial networks. Our study highlights how eco-evolutionary feedbacks can be understood in light of spatial network structure by linking network topology to classical evolutionary mechanisms such as kin selection.

Species are often treated as evolutionarily significant units of diversity that reflect patterns of gene flow and selection. In contrast, higher taxa are mostly regarded as convenient labels for levels in the tree of life, which reflect evolutionary history if defined cladistically but are assumed to have no real significance for ongoing evolution. We test the alternative hypothesis that some higher taxa are evolutionarily significant units with coherent patterns of selection on their constituent species. Specifically, we ask whether the big 4 orders of holometabolous insects, namely Coleoptera, Diptera, Hymenoptera, and Lepidoptera, display divergent, but internally conserved patterns of selection acting on protein-coding genes. Analyzing orthologous genes from whole genome sequence data for multiple species per order, we find that, in most genes, selection on roughly one fifth of codons is conserved within each order but differs significantly among orders. The shift is associated with variation in GC content among orders, but primarily at codon 2nd positions hence due to selection rather than mutational or repair bias. Comparison of alternative models assigning different taxonomic levels (either more lumped or divided than orders) shows that best models always specify Hymenoptera and Lepidoptera as coherent units, whereas patterns of selection on protein-coding genes within Coleoptera and especially Diptera are better explained by subdividing them further. We hypothesise that some aspect of the general lifestyle, body plan or genetic makeup of orders (or of nested clades within Coleoptera and Diptera) leads to conserved patterns of selection across protein-coding genes within them, whereas constraints differ among them. The emergence of whole-genome data for broad and deep phylogenetic samples will allow this hypothesis of evolutionarily significant higher taxa versus more evenly dispersed shifts in selection across genes to be tested further.

Animals living in cities are smaller than their conspecifics from rural areas but whether such differences are caused by genetic differences or food constraints remains untested. We performed a multi-generation common garden study where we raised great tits (Parus major), originating from eggs collected from multiple Dutch cities and forests under the same conditions for two generations. Offspring from city birds had a smaller tarsus than forest birds in both generations, demonstrating that these morphological differences are genetic. Next, we tested whether size differences are an adaptation to the low food abundance when offspring are raised in the city. Third-generation birds of both origins were given food amounts mimicking being raised in forests or cities during the second part of their nestling development. While the treatment resulted in birds in the lower feeding frequency treatment to be smaller, city and forest birds responded the same way, suggesting that city birds do not cope better with reduced food availability. Our study shows that the smaller size of urban birds has a genetic basis and is not only caused by a plastic response to restricted resources in the urban environment. Our experiment does not provide evidence that these genetic differences have evolved as an adaptive response to a reduced food availability in cities.

Dispersal between heterogenous habitats is a major determinant of population diversification, and may often introduce new morphotypes in habitats where population diversity is low. Natural enemies are also key factors affecting the diversification of victim populations. Co-dispersal of enemies may induce local diversity loss at diversity cold spots as enemies from diversity hots pots are often more efficient in predation. Here, we experimentally tested this hypothesis using a model microbial system: Pseudomonas fluorescens and its lytic phage. The ancestral bacterium diversified at three resource levels across eight temperature gradients in the presence and absence of phages. Bacteria diversified into more morphotypes at higher temperatures and higher resource levels when phages are absent, and dispersal increased population local diversity at low-diversity habitats. The presence of phages removed the differences in morphological diversity among different temperatures or resource levels. In addition, the co-dispersal of enemies caused higher morphotype loss at lower-quality habitats where the local bacteria are of lower resistance. The simultaneous dispersal of enemies and victims may have crucial consequences for population persistence in edge habitats.

Theory predicts that the sex ratio within populations should influence the strength of sexual selection, and sex ratio is often used as a proxy for sexual selection. However, recent studies challenge this relationship. We manipulated adult sex ratios in Drosophila melanogaster to comprehensively investigate the relationship between sex ratio and sexual selection. Consistent with theory, we found stronger sexual selection in males than females and an increased variance in male reproductive success (the opportunity for selection) in male-biased sex ratios. In addition, males faced more intense sperm competition in male-biased sex ratios, although the structure of sexual networks was largely invariant to sex ratio. Despite this, we show that sex ratios did not influence sexual selection in males as measured by the Bateman gradient. We leverage randomized null models to reconcile these results and show that the higher male reproductive variance in male-biased sex ratios may be explained by random chance in mating, rather than competitive mechanisms. Our findings indicate that caution is warranted over the long-standing assumption that sex ratio bias is a good proxy for the strength of sexual selection.

Our ability to predict the emergence of novel viruses relies on there being generalizable patterns in the susceptibilities of hosts to novel infections. Studies investigating variation in susceptibility among host species have consistently shown that closely related hosts share similar susceptibilities to a given virus. However, the extent to which such phylogenetic patterns of susceptibility are correlated among diverse sets of viruses is unclear. Here, we investigate phylogenetic correlations in susceptibility among Drosophilidae hosts to a panel of 11 different invertebrate viruses, comprising 7 unique virus species, 6 unique families, and both RNA and DNA viruses. The susceptibility of hosts to each pair of viruses tested was either positively correlated across host species or did not show evidence of correlation. No negative correlations, indicative of evolutionary trade-offs in host susceptibility to different viruses, were detected between any virus pairs. The strength of correlations was generally higher in viruses of the same species and family, consistent with virus phylogenetic patterns in host infectivity. Our results suggest that generalized host susceptibility can result in positive correlations, even between highly diverged viruses, while specialized interactions with individual viruses cause a stepwise decrease in correlation strength between viruses from the within-species, to the within-family, and to the across-family level.

Vision is a complex sensory system that requires coordination among cellular and morphological traits, and it remains unclear how functional relationships among traits interact with ecological selective pressures to shape the evolution of vision. Many species have specialized high visual acuity regions in the retina defined by patterns of ganglion cell density, which may evolve in response to ecological traits. For example, ganglion cell density can increase radially towards the center of the retina to form an area centralis, which is thought to improve acuity towards the center of the visual field in predators. Another example is the horizontal streak, where ganglion cells are dense in a horizontal pattern across the retina, which is thought to be beneficial in horizon-dominated habitats. At the morphological level, many have proposed that predation selects for high orbit convergence angles, or forward-facing eyes. We tested these hypotheses in a phylogenetic framework across eutherian mammals and found support for the association between the horizontal streak and horizon-dominated habitats. However, we did not find a significant association between orbit convergence and predation. We also tested if retinal specializations evolve in response to orbit convergence angles. We found that horizontal streaks were associated with side-facing eyes, potentially facilitating panoramic vision. Previous studies observed that some species with side-facing eyes have an area centralis shifted towards the temporal side of the retina, such that the high acuity region would project forward, but this relationship had not been tested quantitatively. We found that the temporal distance of the area centralis from the center of the retina was inversely correlated with orbit convergence, as predicted. Our work shows a strong relationship between orbit convergence and retinal specializations. We find support that both visual ecology and functional interactions among traits play important roles in the evolution of ocular traits across mammals.

Environmental stress can exacerbate inbreeding depression by amplifying differences between inbred and outbred individuals. In wild populations, where the environment is often unpredictable and stress can be highly detrimental, the interplay between inbreeding depression and environmental variation is potentially important. Here, we investigate variation in inbreeding level, fitness and strength of inbreeding depression across a fine-scale geographic area (~12 km²) in an individually monitored population of red deer (Cervus elaphus). We show that northern regions of the study area have lower birth weights, lower juvenile survival rates, and higher inbreeding coefficients. Such fine-scale differences in inbreeding coefficients could be caused by the mating system of red deer combined with female density variation. We then tested for an inbreeding depression-by-environment interaction (ID × E) in birth weight and juvenile survival, by fitting an interaction term between the inbreeding coefficient and geographic location. We find that inbreeding depression in juvenile survival is stronger in the harsher northern regions, indicating the presence of ID × E. We also highlight that the ability to infer ID × E is affected by the variation in inbreeding within each geographic region. Therefore, for future studies on ID × E in wild populations, we recommend first assessing whether inbreeding and traits vary spatially or temporally. Overall, this is one of only a handful of studies to find evidence for ID × E in a wild population-despite its prevalence in experimental systems-likely due to intense data demands or insufficient variation in environmental stress or inbreeding coefficients.

Male reproductive senescence is typically characterized by a decline in the number of sperm produced and transferred by old males, a phenomenon that may be exacerbated in polygynous species where males mate multiply. However, males also transfer seminal fluid to females, and little is known about its role in modulating male reproductive senescence. Here, we explore the contributions of sperm and seminal fluid towards male reproductive senescence in a series of sequential matings, using Drosophila melanogaster. As expected, old males produce fewer offspring than young males. However, this pattern is not driven by sperm limitation: old males have more sperm and transfer similar numbers to females, compared to young males. Instead, females storing fewer sperm of old males compared to that of young males, over a long term, drives male reproductive senescence. We are able to mitigate the age-related decline in male reproductive output by supplementing females with the seminal fluid of a young male, before she mates with an old male. Similarly, we alleviate the reduction in reproductive output across sequential matings by supplementing females with seminal fluid. Our findings highlight that seminal fluid, rather than sperm number, limits reproductive success in old or multiply mating males, highlighting its underappreciated role in reproductive aging.