Adaptive capabilities and fitness consequences associated with pollution exposure in fish

Many fish populations are exposed to harmful levels of chemical pollution and selection pressures associated with these exposures have led to the evolution of tolerance. Our understanding of the physiological basis for these adaptations is limited, but they are likely to include processes involved with the absorption, distribution, metabolism and/or excretion of the target chemical. Other potential adaptive mechanisms include enhancements in antioxidant responses, an increased capacity for DNA and/or tissue repair and alterations to the life cycle of fish that enable earlier reproduction. Analysis of single-nucleotide polymorphism frequencies has shown that tolerance to hydrocarbon pollutants in both marine and estuarine fish species involves alteration in the expression of the xenobiotic metabolism enzyme CYP1A. In this review, we present novel data showing also that variants of the CYP1A gene have been under selection in guppies living in Trinidadian rivers heavily polluted with crude oil. Potential costs associated with these adaptations could reduce fitness in unpolluted water conditions. Integrating knowledge of local adaptation to pollution is an important future consideration in conservation practices such as for successful restocking, and improving connectivity within river systems. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences’

Evolutionary genomics can improve prediction of species' responses to climate change

Global climate change (GCC) increasingly threatens biodiversity through the loss of species, and the transformation of entire ecosystems. Many species are challenged by the pace of GCC because they might not be able to respond fast enough to changing biotic and abiotic conditions. Species can respond either by shifting their range, or by persisting in their local habitat. If populations persist, they can tolerate climatic changes through phenotypic plasticity, or genetically adapt to changing conditions depending on their genetic variability and census population size to allow for de novo mutations. Otherwise, populations will experience demographic collapses and species may go extinct. Current approaches to predicting species responses to GCC begin to combine ecological and evolutionary information for species distribution modelling. Including an evolutionary dimension will substantially improve species distribution projections which have not accounted for key processes such as dispersal, adaptive genetic change, demography, or species interactions. However, eco-evolutionary models require new data and methods for the estimation of a species' adaptive potential, which have so far only been available for a small number of model species. To represent global biodiversity, we need to devise large-scale data collection strategies to define the ecology and evolutionary potential of a broad range of species, especially of keystone species of ecosystems. We also need standardized and replicable modelling approaches that integrate these new data to account for eco-evolutionary processes when predicting the impact of GCC on species' survival. Here, we discuss different genomic approaches that can be used to investigate and predict species responses to GCC. This can serve as guidance for researchers looking for the appropriate experimental setup for their particular system. We furthermore highlight future directions for moving forward in the field and allocating available resources more effectively, to implement mitigation measures before species go extinct and ecosystems lose important functions

Causes of maladaptation

Evolutionary biologists tend to approach the study of the natural world within a framework of adaptation, inspired perhaps by the power of natural selection to produce fitness advantages that drive population persistence and biological diversity. In contrast, evolution has rarely been studied through the lens of adaptation's complement, maladaptation. This contrast is surprising because maladaptation is a prevalent feature of evolution: population trait values are rarely distributed optimally; local populations often have lower fitness than imported ones; populations decline; and local and global extinctions are common. Yet we lack a general framework for understanding maladaptation; for instance in terms of distribution, severity, and dynamics. Similar uncertainties apply to the causes of maladaptation. We suggest that incorporating maladaptation-based perspectives into evolutionary biology would facilitate better understanding of the natural world. Approaches within a maladaptation framework might be especially profitable in applied evolution contexts – where reductions in fitness are common. Toward advancing a more balanced study of evolution, here we present a conceptual framework describing causes of maladaptation. As the introductory article for a Special Feature on maladaptation, we also summarize the studies in this Issue, highlighting the causes of maladaptation in each study. We hope that our framework and the papers in this Special Issue will help catalyze the study of maladaptation in applied evolution, supporting greater understanding of evolutionary dynamics in our rapidly changing world

Lichen holobionts show compositional structure along elevation

Holobionts are dynamic ecosystems that may respond to abiotic drivers with compositional changes. Uncovering elevational diversity patterns within these microecosystems can further our understanding of community-environment interactions. Here, we assess how the major components of lichen holobionts-fungal hosts, green algal symbionts, and the bacterial community-collectively respond to an elevational gradient. We analyse populations of two lichen symbioses, Umbilicaria pustulata and U. hispanica, along an elevational gradient spanning 2100 altitudinal metres and covering three major biomes. Our study shows (i) discontinuous genomic variation in fungal hosts with one abrupt genomic differentiation within each of the two host species, (ii) altitudinally structured bacterial communities with pronounced turnover within and between hosts, and (iii) altitude-specific presence of algal symbionts. Alpha diversity of bacterial communities decreased with increasing elevation. A marked turnover in holobiont diversity occurred across two altitudinal belts: at 11 degrees C-13 degrees C average annual temperature (here: 800-1200 m a.s.l.), and at 7 degrees C-9 degrees C average annual temperature (here: 1500-1800 m a.s.l.). The two observed zones mark a clustering of distribution limits and community shifts. The three ensuing altitudinal classes, that is, the most frequent combinations of species in holobionts, approximately correspond to the Mediterranean, cool-temperate, and alpine climate zones. We conclude that multitrophic microecosystems, such as lichen holobionts, respond with concerted compositional changes to climatic factors that also structure communities of macroorganisms, for example, vascular plants

Data from: Parting ways: Parasite release in nature leads to sex-specific evolution of defense

We evaluate the extent to which males and females evolve along similar or different trajectories in response to the same environmental shift. Specifically, we use replicate experimental introductions in nature to consider how release from a key parasite (Gyrodactylus) generates similar or different defense evolution in male versus female guppies (Poecilia reticulata). After 8-12 generations of evolution, guppies were collected from the ancestral (parasite still present) and derived (parasite now absent) populations and bred for two generations in the laboratory to control for non-genetic effects. These F2 guppies were then individually infected with Gyrodactylus and infection dynamics were monitored on each fish. We found that parasite release in nature led to sex-specific evolutionary responses: males did not show much evolution of resistance, whereas females showed the evolution of increased resistance. Given that male guppies in the ancestral population had greater resistance to Gyrodactylus than did females, evolution in the derived populations led to reduction of sexual dimorphism in resistance. We argue that previous selection for high resistance in males constrained (relative to females) further evolution of the trait. We advocate more experiments considering sex-specific evolutionary responses to environmental change

Data from: How parallel is parallel evolution? A comparative analysis in fishes

Evidence of phenotypic parallelism is often used to infer the deterministic role played by natural selection. However, variation in the extent or direction of divergence is often evident among independent evolutionary replicates, raising the following question: just how parallel, overall, is parallel evolution? We answer this question through a comparative analysis of studies of fishes, a taxon where parallel evolution has been much discussed. We first ask how much of the among-population variance in phenotypic traits can be explained by different “environment” types, such as high predation versus low predation or benthic versus limnetic. We then use phenotypic change vector analysis to quantify variation in the direction (vector angles) and magnitude (vector lengths) of environment-associated divergence. All analyses show high variation in the extent of parallelism—from very high to very low, along with everything in between—highlighting the importance of quantifying parallelism rather than just asserting its presence. Interestingly, instances of low extents of parallelism represent important components of divergence in many cases, promising considerable opportunities for inferences about the factors shaping phenotypic divergence

Aphids do not attend to leaf colour as visual signal, but to the handicap of reproductive investment

The evolution of visual warning signals is well known in animals but has received scant attention in plants. The coevolutionary hypothesis is the most influential hypothesis on warning signals in plants proposing that red and yellow leaf colours in autumn signal defensive strength to herbivores. So far, evidence in support of the hypothesis, which assumes a coevolutionary origin of autumnal leaf colours, is correlative and open to alternative explanations. We therefore tested the coevolutionary hypothesis experimentally by colouring the leaves either red or green of same-aged mountain ash (Sorbus aucuparia) individuals. We monitored the response of winged aphids to leaf colour using insect glue on branches with natural and artificial leaf colours in each individual. In contrast to the prediction of the coevolutionary hypothesis, aphid numbers did not differ between the individuals with artificial green or artificial red leaves. Likewise, at the within-plant level, aphids did not colonize branches with natural green leaves preferentially. However, we suggest that plants emitted warning signals because aphids colonized the hosts non-randomly. We found a strong positive correlation between aphid numbers and fruit production, suggesting an allocation trade-off between investment in plant defence and reproduction. Our study demonstrates that aphids use warning signals or cues in host selection, probably volatiles, but that they did not use leaf colour

Data from: Quantifying the climatic niche of symbiont partners in a lichen symbiosis indicates mutualist-mediated niche expansions

The large distributional areas and ecological niches of many lichenized fungi may in part be due to the plasticity in interactions between the fungus (mycobiont) and its algal or cyanobacterial partners (photobionts). On the one hand, broad-scale phylogenetic analyses show that partner compatibility in lichens is rather constrained and shaped by reciprocal selection pressures and codiversification independent of ecological drivers. On the other hand, sub-species-level associations among lichen symbionts appear to be environmentally structured rather than phylogenetically constrained. In particular, switching between photobiont ecotypes with distinct environmental preferences has been hypothesized as an adaptive strategy for lichen-forming fungi to broaden their ecological niche. The extent and direction of photobiont-mediated range expansions in lichens, however, have not been examined comprehensively at a broad geographic scale. Here we investigate the population genetic structure of Lasallia pustulata symbionts at sub-species-level resolution across the mycobiont's Europe-wide range, using fungal MCM7 and algal ITS rDNA sequence markers. We show that variance in occurrence probabilities in the geographic distribution of genetic diversity in mycobiont-photobiont interactions is closely related to changes in climatic niches. Quantification of niche extent and overlap based on species distribution modeling and construction of Hutchinsonian climatic hypervolumes revealed that combinations of fungal-algal interactions change at the sub-species level along latitudinal temperature gradients and in Mediterranean climate zones. Our study provides evidence for symbiont-mediated niche expansion in lichens. We discuss our results in the light of symbiont polymorphism and partner switching as potential mechanisms of environmental adaptation and niche evolution in mutualisms

Expanding the mutualistic niche: parallel symbiont turnover along climatic gradients

Keystone mutualisms, such as corals, lichens or mycorrhizae, sustain fundamental ecosystem functions. Range dynamics of these symbioses are, however, inherently difficult to predict because host species may switch between different symbiont partners in different environments, thereby altering the range of the mutualism as a functional unit. Biogeographic models of mutualisms thus have to consider both the ecological amplitudes of various symbiont partners and the abiotic conditions that trigger symbiont replacement. To address this challenge, we here investigate 'symbiont turnover zones'--defined as demarcated regions where symbiont replacement is most likely to occur, as indicated by overlapping abundances of symbiont ecotypes. Mapping the distribution of algal symbionts from two species of lichen-forming fungi along four independent altitudinal gradients, we detected an abrupt and consistent β-diversity turnover suggesting parallel niche partitioning. Modelling contrasting environmental response functions obtained from latitudinal distributions of algal ecotypes consistently predicted a confined altitudinal turnover zone. In all gradients this symbiont turnover zone is characterized by approximately 12°C average annual temperature and approximately 5°C mean temperature of the coldest quarter, marking the transition from Mediterranean to cool temperate bioregions. Integrating the conditions of symbiont turnover into biogeographic models of mutualisms is an important step towards a comprehensive understanding of biodiversity dynamics under ongoing environmental change

Data from: Linking macro-trends and micro-rates: re-evaluating micro-evolutionary support for Cope’s rule

Cope's rule, wherein a lineage increases in body size through time, was originally motivated by macro-evolutionary patterns observed in the fossil record. More recently, some authors have argued that evidence exists for generally positive selection on individual body size in contemporary populations, providing a micro-evolutionary mechanism for Cope's rule. If larger body size confers individual fitness advantages as the selection estimates suggest, thereby explaining Cope's rule, then body size should increase over micro-evolutionary time scales. We test this corollary by assembling a large database of studies reporting changes in phenotypic body size through time in contemporary populations, as well as studies reporting average breeding values for body size through time. Trends in body size were quite variable with an absence of any general trend, and many populations trended toward smaller body sizes. Although selection estimates appear to support Cope's rule, our results suggest that actual rates of phenotypic change for body size do not. We discuss potential reasons for this discrepancy and its implications for the understanding of Cope's rule