Does thermal plasticity align with local adaptation? An interspecific comparison of wing morphology in sepsid flies

Although genetic and plastic responses are sometimes considered as unrelated processes, their phenotypic effects may often align because genetic adaptation is expected to mirror phenotypic plasticity if adaptive, but run counter to it when maladaptive. Because the magnitude and direction of this alignment has further consequences for both the tempo and mode of adaptation, they are relevant for predicting an organisms’ reaction to environmental change. To better understand the interplay between phenotypic plasticity and genetic change in mediating adaptive phenotypic variation to climate variability, we here quantified genetic latitudinal variation and thermal plasticity in wing loading and wing shape in two closely related and widespread sepsid flies. Common garden rearing of 16 geographical populations reared across multiple temperatures revealed that wing loading decreases with latitude in both species. This pattern could be driven by selection for increased dispersal capacity in the cold. However, although allometry, sexual dimorphism, thermal plasticity and latitudinal differentiation in wing shape all show similar patterns in the two species, the relationship between the plastic and genetic responses differed between them. Although latitudinal differentiation (south to north) mirrored thermal plasticity (hot to cold) in Sepsis punctum, there was no relationship in Sepsis fulgens. While this suggests that thermal plasticity may have helped to mediate local adaptation in S. punctum, it also demonstrates that genetic wing shape differentiation and its relation to thermal plasticity may be complex and idiosyncratic, even among ecologically similar and closely related species. Hence, genetic responses can, but do not necessarily, align with phenotypic plasticity induced by changing environmental selection pressures.     

油松天然群体的种实性状表型多样性研究

为了揭示油松天然种群在不同地理环境条件下表型变异的程度和规律,在油松整个天然分布范围内选择了12个具有代表性的居群作为研究对象,对其球果、种子、种翅等12个种实性状的变异程度及其与环境因子间关系进行了比较分析。结果显示:(1)各个性状在居群内和居群间均存在较大的变异(CV>12%)。其中千山(QS),曾家镇(ZJ)和互助(HZ)3个居群表现出了较高的变异(CV>20%),而球果干重(CDW)和种子长(CL)是所有表型性状中变异幅度最大的(CV分别为31%和21%),但种翅性状与其他性状相比具有较高的稳定性。(2)巢式设计方差分析表明,在居群内表型分化系数(Vst)变化在3.18%~89.86%之间,而群体间的Vst为38.97%;与其他针叶树种相比,油松拥有较高的表型分化系数,且居群内的变异程度远高于居群间的变异,尤其是千山(QS)、曾家镇(ZJ)和互助(HZ)3个居群,这说明油松具有较高的环境异质性适应能力或恶劣环境耐受能力。(3)相关性分析表明,该研究的各形态特征与潜在蒸发量均为负相关,且大部分形态指标间及它们与潜在蒸发量间存在显著相关性,表明潜在蒸发量是油松形态特征变化的最重要环境影响因子,预示油松最适宜生长于温暖潮湿的环境中;并表明因各形态特征间相互紧密关联,所以它们受环境条件影响而共变。     

Subtle but ubiquitous selection on body size in a natural population of collared flycatchers over 33 years

Understanding the magnitude and long‐term patterns of selection in natural populations is of importance, for example, when analysing the evolutionary impact of climate change. We estimated univariate and multivariate directional, quadratic and correlational selection on four morphological traits (adult wing, tarsus and tail length, body mass) over a time period of 33 years (≈ 19 000 observations) in a nest‐box breeding population of collared flycatchers (Ficedula albicollis). In general, selection was weak in both males and females over the years regardless of fitness measure (fledged young, recruits and survival) with only few cases with statistically significant selection. When data were analysed in a multivariate context and as time series, a number of patterns emerged; there was a consistent, but weak, selection for longer wings in both sexes, selection was stronger on females when the number of fledged young was used as a fitness measure, there were no indications of sexually antagonistic selection, and we found a negative correlation between selection on tarsus and wing length in both sexes but using different fitness measures. Uni‐ and multivariate selection gradients were correlated only for wing length and mass. Multivariate selection gradient vectors were longer than corresponding vector of univariate gradients and had more constrained direction. Correlational selection had little importance. Overall, the fitness surface was more or less flat with few cases of significant curvature, indicating that the adaptive peak with regard to body size in this species is broader than the phenotypic distribution, which has resulted in weak estimates of selection.     

Quantitative Assessment of the Importance of Phenotypic Plasticity in Adaptation to Climate Change in Wild Bird Populations

Predictions about the fate of species or populations under climate change scenarios typically neglect adaptive evolution and phenotypic plasticity, the two major mechanisms by which organisms can adapt to changing local conditions. As a consequence, we have little understanding of the scope for organisms to track changing environments by in situ adaptation. Here, we use a detailed individual-specific long-term population study of great tits (Parus major) breeding in Wytham Woods, Oxford, UK to parameterise a mechanistic model and thus directly estimate the rate of environmental change to which in situ adaptation is possible. Using the effect of changes in early spring temperature on temporal synchrony between birds and a critical food resource, we focus in particular on the contribution of phenotypic plasticity to population persistence. Despite using conservative estimates for evolutionary and reproductive potential, our results suggest little risk of population extinction under projected local temperature change; however, this conclusion relies heavily on the extent to which phenotypic plasticity tracks the changing environment. Extrapolating the model to a broad range of life histories in birds suggests that the importance of phenotypic plasticity for adjustment to projected rates of temperature change increases with slower life histories, owing to lower evolutionary potential. Understanding the determinants and constraints on phenotypic plasticity in natural populations is thus crucial for characterising the risks that rapidly changing environments pose for the persistence of such populations.     

Phenotypic plasticity of body size in Drosophila: effects of a daily periodicity of growth temperature in two sibling species

Abstract. Variation of wing and thorax length under thermoperiodic growth conditions was analysed in four strains of two sibling species, Drosophila melanogaster and D. simulans , from two European localities. Results were compared to those obtained with constant temperatures ranging from 12 to 31 °C.
Under constant temperatures the data basically confirmed previous results: concave reaction norms for wing and thorax length; a monotonically decreasing norm for wing : thorax ratio; and an increasing norm for sex dimorphism (female : male ratio). Phenotypic variability was maximum at extreme temperatures and minimum at middle ones. Slight differences were observed according to the geographical origin: the difference between strains from Bordeaux (France) and Cordoba (Spain) was maximum at low temperatures but disappeared at about 28 °C.
According to the temperatures chosen, alternating thermal regimens had either no effect or produced a significant size reduction, probably reflecting a periodic stress. The magnitude of this effect was proportional to the amplitude of the thermoperiod but not to the quality (cold or heat) of the stress. In a similar way, the wing : thorax ratio was either not modified or reduced significantly, indicating that wing length was relatively more affected than thorax length by alternating thermal regimens. Sex dimorphism also showed either no change or a significant increase, indicating that males were relatively more reactive than females to alternating conditions. Finally, regimens of broad amplitudes increased the phenotypic variability, again an indication of stressful effects. All these observations should be taken into account when analysing phenotypic variability in nature and trying to understand natural selection in wild-living populations.     

Plasticity in functional traits in the context of climate change: a case study of the subalpine forb Boechera stricta (Brassicaceae)

Environmental variation often induces shifts in functional traits, yet we know little about whether plasticity will reduce extinction risks under climate change. As climate change proceeds, phenotypic plasticity could enable species with limited dispersal capacity to persist in situ, and migrating populations of other species to establish in new sites at higher elevations or latitudes. Alternatively, climate change could induce maladaptive plasticity, reducing fitness, and potentially stalling adaptation and migration. Here, we quantified plasticity in life history, foliar morphology, and ecophysiology in Boechera stricta (Brassicaceae), a perennial forb native to the Rocky Mountains. In this region, warming winters are reducing snowpack and warming springs are advancing the timing of snow melt. We hypothesized that traits that were historically advantageous in hot and dry, low‐elevation locations will be favored at higher elevation sites due to climate change. To test this hypothesis, we quantified trait variation in natural populations across an elevational gradient. We then estimated plasticity and genetic variation in common gardens at two elevations. Finally, we tested whether climatic manipulations induce plasticity, with the prediction that plants exposed to early snow removal would resemble individuals from lower elevation populations. In natural populations, foliar morphology and ecophysiology varied with elevation in the predicted directions. In the common gardens, trait plasticity was generally concordant with phenotypic clines from the natural populations. Experimental snow removal advanced flowering phenology by 7 days, which is similar in magnitude to flowering time shifts over 2–3 decades of climate change. Therefore, snow manipulations in this system can be used to predict eco‐evolutionary responses to global change. Snow removal also altered foliar morphology, but in unexpected ways. Extensive plasticity could buffer against immediate fitness declines due to changing climates.     

Climate envelope modelling reveals intraspecific relationships among flowering phenology, niche breadth and potential range size in Arabidopsis thaliana

Species often harbour large amounts of phenotypic variation in ecologically important traits, and some of this variation is genetically based. Understanding how this genetic variation is spatially structured can help to understand species' ecological tolerances and range limits. We modelled the climate envelopes of Arabidopsis thaliana genotypes, ranging from early- to late-flowering, as a function of several climatic variables. We found that genotypes with contrasting alleles at individual flowering time loci differed significantly in potential range size and niche breadth. We also found that later flowering genotypes had more restricted range potentials and narrower niche breadths than earlier flowering genotypes, indicating that local selection on flowering can constrain or enhance the ability of populations to colonise other areas. Our study demonstrates how climate envelope models that incorporate ecologically important genetic variation can provide insights into the macroecology of a species, which is important to understand its responses to changing environments.     

Plant adaptation to climate change—Where are we?

Climate change poses critical challenges for population persistence in natural communities, for agriculture and environmental sustainability, and for food security. In this review, we discuss recent progress in climatic adaptation in plants. We evaluate whether climate change exerts novel selection and disrupts local adaptation, whether gene flow can facilitate adaptive responses to climate change, and whether adaptive phenotypic plasticity could sustain populations in the short term. Furthermore, we discuss how climate change influences species interactions. Through a more in‐depth understanding of these eco‐evolutionary dynamics, we will increase our capacity to predict the adaptive potential of plants under climate change. In addition, we review studies that dissect the genetic basis of plant adaptation to climate change. Finally, we highlight key research gaps, ranging from validating gene function to elucidating molecular mechanisms, expanding research systems from model species to other natural species, testing the fitness consequences of alleles in natural environments, and designing multifactorial studies that more closely reflect the complex and interactive effects of multiple climate change factors. By leveraging interdisciplinary tools (e.g., cutting‐edge omics toolkits, novel ecological strategies, newly developed genome editing technology), researchers can more accurately predict the probability that species can persist through this rapid and intense period of environmental change, as well as cultivate crops to withstand climate change, and conserve biodiversity in natural systems.     

Declining body sizes in North American birds associated with climate change

Recent climate change has caused comparatively rapid shifts in the phenology and geographic distributions of many plants and animals. However, there is debate over the degree to which populations can meet the challenges of climate change with evolutionary or phenotypic responses in life history and morphology. We report that migrating birds captured at a banding station in western Pennsylvania, USA, have exhibited steadily decreasing fat‐free mass and wing chord since 1961, consistent with a response to a warmer climate. This confirms that phenotypic responses to climate change are currently underway in entire avian assemblages. Declines in body size were not explained by an index of habitat condition within the breeding or wintering distributions. Instead, size was negatively correlated with temperature in the previous year, and long‐term trends were associated with the direction of natural selection acting on size over the winter: species undergoing the strongest selection favoring small wing chord showed the most rapid long‐term declines in wing. Phenotypic changes are therefore in line with the prevailing selection regime.     

Adaptive and nonadaptive plasticity in changing environments: Implications for sexual species with different life history strategies

Populations adapt to novel environmental conditions by genetic changes or phenotypic plasticity. Plastic responses are generally faster and can buffer fitness losses under variable conditions. Plasticity is typically modeled as random noise and linear reaction norms that assume simple one‐to‐one genotype–phenotype maps and no limits to the phenotypic response. Most studies on plasticity have focused on its effect on population viability. However, it is not clear, whether the advantage of plasticity depends solely on environmental fluctuations or also on the genetic and demographic properties (life histories) of populations. Here we present an individual‐based model and study the relative importance of adaptive and nonadaptive plasticity for populations of sexual species with different life histories experiencing directional stochastic climate change. Environmental fluctuations were simulated using differentially autocorrelated climatic stochasticity or noise color, and scenarios of directional climate change. Nonadaptive plasticity was simulated as a random environmental effect on trait development, while adaptive plasticity as a linear, saturating, or sinusoidal reaction norm. The last two imposed limits to the plastic response and emphasized flexible interactions of the genotype with the environment. Interestingly, this assumption led to (a) smaller phenotypic than genotypic variance in the population (many‐to‐one genotype–phenotype map) and the coexistence of polymorphisms, and (b) the maintenance of higher genetic variation—compared to linear reaction norms and genetic determinism—even when the population was exposed to a constant environment for several generations. Limits to plasticity led to genetic accommodation, when costs were negligible, and to the appearance of cryptic variation when limits were exceeded. We found that adaptive plasticity promoted population persistence under red environmental noise and was particularly important for life histories with low fecundity. Populations producing more offspring could cope with environmental fluctuations solely by genetic changes or random plasticity, unless environmental change was too fast.     

Trait‐specific consequences of inbreeding on adaptive phenotypic plasticity

Environmental changes may stress organisms and stimulate an adaptive phenotypic response. Effects of inbreeding often interact with the environment and can decrease fitness of inbred individuals exposed to stress more so than that of outbred individuals. Such an interaction may stem from a reduced ability of inbred individuals to respond plastically to environmental stress; however, this hypothesis has rarely been tested. In this study, we mimicked the genetic constitution of natural inbred populations by rearing replicate Drosophila melanogaster populations for 25 generations at a reduced population size (10 individuals). The replicate inbred populations, as well as control populations reared at a population size of 500, were exposed to a benign developmental temperature and two developmental temperatures at the lower and upper margins of their viable range. Flies developed at the three temperatures were assessed for traits known to vary across temperatures, namely abdominal pigmentation, wing size, and wing shape. We found no significant difference in phenotypic plasticity in pigmentation or in wing size between inbred and control populations, but a significantly higher plasticity in wing shape across temperatures in inbred compared to control populations. Given that the norms of reaction for the noninbred control populations are adaptive, we conclude that a reduced ability to induce an adaptive phenotypic response to temperature changes is not a general consequence of inbreeding and thus not a general explanation of inbreeding–environment interaction effects on fitness components.     

Shrinking before our isles: the rapid expression of insular dwarfism in two invasive populations of guttural toad (Sclerophrys gutturalis)

Island ecosystems have traditionally been hailed as natural laboratories for examining phenotypic change, including dramatic shifts in body size. Similarly, biological invasions can drive rapid localized adaptations within modern timeframes. Here, we compare the morphology of two invasive guttural toad (Sclerophrys gutturalis) populations in Mauritius and Réunion with their source population from South Africa. We found that female toads on both islands were significantly smaller than mainland counterparts (33.9% and 25.9% reduction, respectively), as were males in Mauritius (22.4%). We also discovered a significant reduction in the relative hindlimb length of both sexes, on both islands, compared with mainland toads (ranging from 3.4 to 9.0%). If our findings are a result of natural selection, then this would suggest that the dramatic reshaping of an amphibian''s morphology—leading to insular dwarfism—can result in less than 100 years; however, further research is required to elucidate the mechanism driving this change (e.g. heritable adaptation, phenotypic plasticity, or an interaction between them).     

Evolution of morphological differences with moderate genetic correlations among traits as exemplified by two flycatcher species (Ficeduia; Muscicapidae)

Theoretical work on multivariate evolution predicts that genetic correlations can act to constrain the rate at which new adaptive peaks are reached, but there is very limited empirical information available on this issue so far. To evaluate the importance of genetic correlations for evolutionary change, we studied the morphological differences between two flycatcher species (Ficeduia albicollis and F. hypoleuca) using both univariate and multivariate quantitative genetic models. Comparison of the results obtained using these different models revealed that even relatively low genetic correlations between traits will considerably increase the net selection forces needed for evolutionary changes in morphology. In particular, the divergence in wing and tail length, which are positively genetically correlated, would require a considerable amount of antagonistic selection. Because of the genetic correlations, strong selection will be needed to retain certain traits unchanged while others are changing. Based on these results, we argue that it is unlikely that small morphological differences such as between these two species could have evolved during a short (200 years) time period, i.e. the period of sympatry of these species in Sweden. These findings support the hypothesis that even relatively low genetic correlations may constrain short-term adaptive evolution in natural populations.     

DISSECTING CORRELATED CHARACTERS: ADAPTIVE ASPECTS OF PHENOTYPIC COVARIATION IN MELANIZATION PATTERN OF PIERIS BUTTERFLIES

In this study we address the question of how much of the covariation among phenotypic characters observed in natural populations is adaptive. We examine covariation among a set of phenotypic characters that describe the wing-melanization pattern of Pieris butterflies. Previous functional analyses of thermoregulatory performance allow us to predict a priori whether and how different wing melanic characters should be correlated. We quantify and analyze the variation in the wing-melanization pattern within species for a series of Pieris populations from relatively cool environments in North America and compare these results with the predictions based on our adaptive hypothesis. We consider adaptive covariation both for biogeographic variation among populations and for seasonal polyphenism (phenotypic plasticity) within populations. Our hypothesis correctly predicts many of the qualitative features of covariation in melanization among major regions of the wings, at the level of biogeographic variation among populations, for both males and females of Pieris occidentalis. When within-population variation is considered, agreement with the adaptive predictions varies considerably in different populations for both P. occidentalis and P. napi males and females. Agreement for P. napi, particularly the females, is generally poorer than for P. occidentalis. In both species, there is a consistent difference in melanization pattern between alpine and arctic sites; this difference is discussed in relation to the differences in the radiative environment between these two types of “cold” habitats. Our results suggest that some important aspects of phenotypic correlation among wing melanic characters in Pieris are adaptive. We emphasize the important distinction between covariation and co-occurrence of characters, and we discuss these results in relation to the extensive biogeographic variation and phenotypic plasticity (seasonal polyphenism) in Pieris wing-melanization patterns.     

PLASTICITY VERSUS ENVIRONMENTAL CANALIZATION: POPULATION DIFFERENCES IN THERMAL RESPONSES ALONG A LATITUDINAL GRADIENT IN DROSOPHILA SERRATA

The phenotypic plasticity of traits, defined as the ability of a genotype to express different phenotypic values of the trait across a range of environments, can vary between habitats depending on levels of temporal and spatial heterogeneity. Other traits can be insensitive to environmental perturbations and show environmental canalization. We tested levels of phenotypic plasticity in diverse Drosophila serrata populations along a latitudinal cline ranging from a temperate, variable climate to a tropical, stable climate by measuring developmental rate and size-related traits at three temperatures (16°C, 22°C, and 28°C). We then compared the slopes of the thermal reaction norms among populations. The 16–22°C part of the reaction norms for developmental rate was flatter (more canalized) for the temperate populations than for the tropical populations. However, slopes for the reaction norms of the two morphological traits (wing size, wing:thorax ratio), were steeper (more plastic) in the temperate versus the tropical populations over the entire thermal range. The different latitudinal patterns in plasticity for developmental rate and the morphological traits may reflect contrasting selection pressures along the tropical–temperate thermal gradient.     

Natural history collections as windows on evolutionary processes

Natural history collections provide an immense record of biodiversity on Earth. These repositories have traditionally been used to address fundamental questions in biogeography, systematics and conservation. However, they also hold the potential for studying evolution directly. While some of the best direct observations of evolution have come from long‐term field studies or from experimental studies in the laboratory, natural history collections are providing new insights into evolutionary change in natural populations. By comparing phenotypic and genotypic changes in populations through time, natural history collections provide a window into evolutionary processes. Recent studies utilizing this approach have revealed some dramatic instances of phenotypic change over short timescales in response to presumably strong selective pressures. In some instances, evolutionary change can be paired with environmental change, providing a context for potential selective forces. Moreover, in a few cases, the genetic basis of phenotypic change is well understood, allowing for insight into adaptive change at multiple levels. These kinds of studies open the door to a wide range of previously intractable questions by enabling the study of evolution through time, analogous to experimental studies in the laboratory, but amenable to a diversity of species over longer timescales in natural populations.     

Role of phenotypic plasticity and population differentiation in adaptation to novel environmental conditions

Species can adapt to new environmental conditions either through individual phenotypic plasticity, intraspecific genetic differentiation in adaptive traits, or both. Wild emmer wheat, Triticum dicoccoides, an annual grass with major distribution in Eastern Mediterranean region, is predicted to experience in the near future, as a result of global climate change, conditions more arid than in any part of the current species distribution. To understand the role of the above two means of adaptation, and the effect of population range position, we analyzed reaction norms, extent of plasticity, and phenotypic selection across two experimental environments of high and low water availability in two core and two peripheral populations of this species. We studied 12 quantitative traits, but focused primarily on the onset of reproduction and maternal investment, which are traits that are closely related to fitness and presumably involved in local adaptation in the studied species. We hypothesized that the population showing superior performance under novel environmental conditions will either be genetically differentiated in quantitative traits or exhibit higher phenotypic plasticity than the less successful populations. We found the core population K to be the most plastic in all three trait categories (phenology, reproductive traits, and fitness) and most successful among populations studied, in both experimental environments; at the same time, the core K population was clearly genetically differentiated from the two edge populations. Our results suggest that (1) two means of successful adaptation to new environmental conditions, phenotypic plasticity and adaptive genetic differentiation, are not mutually exclusive ways of achieving high adaptive ability; and (2) colonists from some core populations can be more successful in establishing beyond the current species range than colonists from the range extreme periphery with conditions seemingly closest to those in the new environment.     

Evidence for intraspecific phenotypic variation in songbirds along elevation gradients in central Europe

Studying phenotypic variations along gradients may provide insights into mechanisms that drive species distributions and thus can be useful indicators of environmental change. In mountains, the study of phenotypic variation along elevation gradients is of increasing relevance due to the impacts of climate change. We analysed European ringing data to measure the direction of phenotypic variation along elevation gradients in six common, resident songbird species occurring along a wide elevational range. We modelled intraspecific change in wing length, body mass and their ratio with elevation and found a significant increase in wing length and a decrease in body mass at high elevations. The results of our exploratory analysis show the potential that continent-wide ringing databases offer to describe patterns of phenotypic variation along environmental gradients.     

Rapid morphological divergence of a stream fish in response to changes in water flow

Recent evidence indicates that evolution can occur on a contemporary time scale. However, the precise timing and patterns of phenotypic change are not well known. Reservoir construction severely alters selective regimes in aquatic habitats due to abrupt cessation of water flow. We examined the spatial and temporal patterns of evolution of a widespread North American stream fish (Pimephales vigilax) in response to stream impoundment. Gross morphological changes occurred in P. vigilax populations following dam construction in each of seven different rivers. Significant changes in body depth, head shape and fin placement were observed relative to fish populations that occupied the rivers prior to dam construction. These changes occurred over a very small number of generations and independent populations exhibited common responses to similar selective pressures. The magnitude of change was observed to be greatest in the first 15 generations post-impoundment, followed by continued but more gradual change thereafter. This pattern suggests early directional selection facilitated by phenotypic plasticity in the first 10–20 years, followed by potential stabilizing selection as populations reached a new adaptive peak (or variation became exhausted). This study provides evidence for rapid, apparently adaptive, phenotypic divergence of natural populations due to major environmental perturbations in a changing world.     

Parasite‐mediated selection in a natural metapopulation of Daphnia magna

Parasite‐mediated selection varying across time and space in metapopulations is expected to result in host local adaptation and the maintenance of genetic diversity in disease‐related traits. However, nonadaptive processes like migration and extinction‐(re)colonization dynamics might interfere with adaptive evolution. Understanding how adaptive and nonadaptive processes interact to shape genetic variability in life‐history and disease‐related traits can provide important insights into their evolution in subdivided populations. Here we investigate signatures of spatially fluctuating, parasite‐mediated selection in a natural metapopulation of Daphnia magna. Host genotypes from infected and uninfected populations were genotyped at microsatellite markers, and phenotyped for life‐history and disease traits in common garden experiments. Combining phenotypic and genotypic data a Q_ST–F_ST‐like analysis was conducted to test for signatures of parasite mediated selection. We observed high variation within and among populations for phenotypic traits, but neither an indication of host local adaptation nor a cost of resistance. Infected populations have a higher gene diversity (Hs) than uninfected populations and Hs is strongly positively correlated with fitness. These results suggest a strong parasite effect on reducing population level inbreeding. We discuss how stochastic processes related to frequent extinction‐(re)colonization dynamics as well as host and parasite migration impede the evolution of resistance in the infected populations. We suggest that the genetic and phenotypic patterns of variation are a product of dynamic changes in the host gene pool caused by the interaction of colonization bottlenecks, inbreeding, immigration, hybrid vigor, rare host genotype advantage and parasitism. Our study highlights the effect of the parasite in ameliorating the negative fitness consequences caused by the high drift load in this metapopulation.