Local Maladaptation Research Articles

Signatures of local adaptation and maladaptation to future climate in wild Zizania latifolia

Global climate change poses challenges to agricultural production and food security. Assessing the adaptive capacity of crop wild relatives to future climate is important for protecting key germplasm resources and breeding new crops. We performed population genomics, genotype-environment association analyses, and genomic offset assessment of Chinese wild rice, Zizania latifolia, a crop wild relative and potential new grain crop, based on 168 individuals from 42 populations. We found two genetic lineages in Z. latifolia, corresponding to the south and north of its range, that diverged during the Late Pleistocene. We also identified lineage-specific positively selected genes associated with flower development and flowering, seed shattering, pathogen defense response and cold tolerance. We further found that populations from southeastern China are the most maladapted to future climate and should be prioritized for conservation. Our findings provide important clues for leveraging existing genetic diversity to identify important germplasm resources and create climate-resilient crops.

Testing source elevation versus genotype as predictors of sugar pine performance in a post‐fire restoration planting

AbstractClimate change is motivating a reassessment of how seeds are selected for reforestation, as rapid environmental change can lead to local maladaptation in trees. Genetic association studies and past seed source climate both have the potential to help identify appropriate planting stock, but these techniques have not been compared and tested as part of an operational planting program. In this study, we combined an analysis of single nucleotide polymorphisms (SNPs) associated with environmental gradients in sugar pine (Pinus lambertiana) with an analysis of post‐fire seedling survival and growth in a restoration experiment. Our genotype–environment association (GEA) tests of 92 individuals from varying climates within CA revealed 829 SNPs (out of 300,604) with significant association with climate gradients, especially April snowpack. Of these, 323 either had annotations that suggested potential functional importance or were identified by two different methods. We then built Bayesian models of survival and growth for all seedlings in a separate post‐fire planting experiment, to test the relative predictive ability of source elevation (a common proxy for source climate) versus the proportion of seedling alleles expected to be locally advantageous based on GEA. Across three sites within the King Fire scar in Eldorado National Forest in 2017, 2018, and 2019, 1774 seedlings were planted. Of these, 206 had enough green needles in 2020 to allow sample collection, and 161 were successfully genotyped. We found that source elevation was generally better at predicting seedling performance than genotype indices, perhaps because of the limited scope of the association analysis. Seed sources from 500 to 1800 ft (152.4–548.6 m) lower in elevation, and one seed zone further south generally performed as well or better than local seed sources. This result, and those of similar previous studies, suggest that “climate matching” using past climate information for existing seed sourcing units is a reasonable starting point for finding seedlings suited to already‐altered planting site climate conditions. However, further tests with more extensive genomic and performance data may improve the utility of genotype information for seed selection.

Short-term fluctuating and long-term divergent selection on sympatric Monkeyflowers: insights from decade-spanning reciprocal transplants.

Sympatric species are often locally adapted to distinct microhabitats. However, temporal variation may cause local maladaptation and species boundary breakdown, especially during extreme climatic events leading to episodic selection. Repeated reciprocal transplants can reveal the interplay between short and long-term patterns of natural selection. To examine evolutionary trajectories of sympatric Monkeyflowers adapted to different niches, Mimulus guttatus and M. laciniatus, we performed three replicated transplants and combined them with previous experiments to leverage a dataset of five transplants spanning 10 years. We performed phenotypic selection analyses on parents and hybrids in parental habitats in Yosemite NP, CA during years of drastically differing snowpack. If there is ecological isolation, then we predicted divergent phenotypic selection between habitats in line with species' differences and local adaptation. We found interannual fluctuations in phenotypic selection, often in unpredicted directions. However, a combined-year analysis detected longer-term divergent selection on flowering time, a key temporally isolating and adaptative trait, suggesting that selection may reinforce species boundaries despite short-term fluctuations. Finally, we found temporal variation in local adaptation with M. laciniatus locally adapted in low snowpack years, while an extremely high snowpack year contributed to average local maladaptation of M. guttatus.

Evolution and plasticity of physiological traits in the collembolan Orchesella villosa at fine spatial scales within the city

Abstract Divergent natural selection caused by spatial environmental variation can lead to local adaptation and evolutionary divergence between populations, even those within close proximity to one another. This, however, is only one possibility among other outcomes, such as the evolution of adaptive phenotypic plasticity or local maladaptation. Cities, as fragmented landscapes with high environmental variability across microgeographic scales, present an excellent venue to explore these possible outcomes. Here, we use common garden experiments to explore the potential for microgeographic divergence of physiological traits among populations of a collembolan, Orchesella villosa, living within the footprint of a single city. We assessed if intra-urban variation in the intensity of the heat island effect and soil salinity has led to evolutionary divergence in heat tolerance and salinity tolerance, respectively. While we found little variation in salinity tolerance among populations, there was evidence for both plasticity and evolutionary divergence among populations in response to variation in the urban heat island. Although the adaptive nature of these specific responses is not known, we suggest that cities, and human modified habitats in general, promote evolutionary divergence at small spatial scales by creating barriers to dispersal and imposing divergent selective environments within previously contiguous habitats.

Patterns of genetic variation and local adaptation of a native herbivore to a lethal invasive plant.

Understanding the evolutionary processes that influence fitness is critical to predicting species' responses to selection. Interactions among evolutionary processes including gene flow, drift and the strength of selection can lead to either local adaptation or maladaptation, especially in heterogenous landscapes. Populations experiencing novel environments or resources are ideal for understanding the mechanisms underlying adaptation or maladaptation, specifically in locally co-evolved interactions. We used the interaction between a native herbivore that oviposits on a patchily distributed introduced plant that in turn causes significant mortality to the larvae to test for signatures of local adaptation in areas where the two co-occurred. We used whole-genome sequencing to explore population structure, patterns of gene flow and signatures of local adaptation. We found signatures of local adaptation in response to the introduced plant in the absence of strong population structure with no genetic differentiation and low genetic variation. Additionally, we found localized allele frequency differences within a single population between habitats with and without the lethal plant, highlighting the effects of strong selection. Finally, we identified that selection was acting on larval ability to feed on the plant rather than on females' ability to avoid oviposition, thus uncovering the specific ontogenetic target of selection. Our work highlights the potential for adaptation to occur in a fine-grained landscape in the presence of gene flow and low genetic variation.

Interpretation issues with "genomic vulnerability" arise from conceptual issues in local adaptation and maladaptation.

As climate change causes the environment to shift away from the local optimum that populations have adapted to, fitness declines are predicted to occur. Recently, methods known as genomic offsets (GOs) have become a popular tool to predict population responses to climate change from landscape genomic data. Populations with a high GO have been interpreted to have a high "genomic vulnerability" to climate change. GOs are often implicitly interpreted as a fitness offset, or a change in fitness of an individual or population in a new environment compared to a reference. However, there are several different types of fitness offset that can be calculated, and the appropriate choice depends on the management goals. This study uses hypothetical and empirical data to explore situations in which different types of fitness offsets may or may not be correlated with each other or with a GO. The examples reveal that even when GOs predict fitness offsets in a common garden experiment, this does not necessarily validate their ability to predict fitness offsets to environmental change. Conceptual examples are also used to show how a large GO can arise under a positive fitness offset, and thus cannot be interpreted as a population vulnerability. These issues can be resolved with robust validation experiments that can evaluate which fitness offsets are correlated with GOs.

A stabilizing eco-evolutionary feedback loop in the wild

There is increasing evidence that evolutionary and ecological processes can operate on the same timescale1,2 (i.e., contemporary time). As such, evolution can be sufficiently rapid to affect ecological processes such as predation or competition. Thus, evolution can influence population, community, and ecosystem-level dynamics. Indeed, studies have now shown that evolutionary dynamics can alter community structure3,4,5,6 and ecosystem function.7,8,9,10 In turn, shifts in ecological dynamics driven by evolution might feed back to affect the evolutionary trajectory of individual species.11 This feedback loop, where evolutionary and ecological changes reciprocally affect one another, is a central tenet of eco-evolutionary dynamics.1,12 However, most work on such dynamics in natural populations has focused on one-way causal associations between ecology and evolution.13 Hence, direct empirical evidence for eco-evolutionary feedback is rare and limited to laboratory or mesocosm experiments.13,14,15,16 Here, we show in the wild that eco-evolutionary dynamics in a plant-feeding arthropod community involve a negative feedback loop. Specifically, adaptation in cryptic coloration in a stick-insect species mediates bird predation, with local maladaptation increasing predation. In turn, the abundance of arthropods is reduced by predation. Here, we experimentally manipulate arthropod abundance to show that these changes at the community level feed back to affect the stick-insect evolution. Specifically, low-arthropod abundance increases the strength of selection on crypsis, increasing local adaptation of stick insects in a negative feedback loop. Our results suggest that eco-evolutionary feedbacks are able to stabilize complex systems by preventing consistent directional change and therefore increasing resilience.

Mutualistic coevolution and community diversity favour persistence in metacommunities under environmental changes.

Linking local to regional ecological and evolutionary processes is key to understand the response of Earth's biodiversity to environmental changes. Here we integrate evolution and mutualistic coevolution in a model of metacommunity dynamics and use numerical simulations to understand how coevolution can shape species distribution and persistence in landscapes varying in space and time. Our simulations show that coevolution and species richness can synergistically shape distribution patterns by increasing colonization and reducing extinction of populations in metacommunities. Although conflicting selective pressures emerging from mutualisms may increase mismatches with the local environment and the rate of local extinctions, coevolution increases trait matching among mutualists at the landscape scale, counteracting local maladaptation and favouring colonization and range expansions. Our results show that by facilitating colonization, coevolution can also buffer the effects of environmental changes, preventing species extinctions and the collapse of metacommunities. Our findings reveal the mechanisms whereby coevolution can favour persistence under environmental changes and highlight that these positive effects are greater in more diverse systems that retain landscape connectivity.

The strength and direction of local (mal)adaptation depends on neighbour density and the environment

Abstract Populations are embedded in communities, but despite their potential to affect individual fitness, it is unknown whether and how species interactions evolve in communities. Evolutionary outcomes are likely more complex in natural communities because (a) the evolution of interactions may not be evenly distributed among all community members and (b) coevolution is conditional on the environmental conditions within which interactions are playing out. To test the evolution of interaction strengths in natural communities, we performed two common garden experiments in grassland communities in Northern California. In each garden, we transplanted individuals of four populations (one local, three foreign) of an annual invasive grass Bromus hordeaceus into natural communities, characterized the interaction neighbourhood around each focal individual, and quantified individual fitness. This method allowed us to fit multispecies competition models to fitness data, estimating interaction strengths between focal B. hordeaceus populations and each of seven species that were common in the interaction neighbourhoods, in each garden. We found that interaction strengths significantly differed among local and foreign source populations, but the direction and magnitude of evolution differed among common gardens and among neighbour species—in neither garden were interactions experienced more strongly by foreign populations compared to local populations. The fitness of local populations (relative to foreign populations) decreased when neighbours were removed, strongly enough in one garden to cause strong local maladaptation, and the local population did not perform the best in either garden. Synthesis. Together, our results demonstrate how species interactions evolve to determine fitness in ecological communities, providing a richer view of adaptation in natural systems. In our study, this richness included the unique challenges populations face in nature: uneven abundances and a diffuseness of species interactions, nonlinear density effects on fitness, and evidence of (mal)adaptation that is conditional on local conditions. We conclude by hypothesizing the causes and consequences of challenges to adaptation and how they help identify priority areas for the field.

Road salt is more toxic to wood frog embryos from polluted ponds

Organisms that rely on aquatic habitats in roaded landscapes face a growing array of consequences from pollution, especially due to freshwater salinization. Critically, these consequences can vary from population to population depending on exposure histories and evolutionary responses. Prior studies using transplant and common garden experiments have found that aquatic-stage wood frogs (Rana sylvatica) from roadside populations are less fit in the wild and more sensitive to road salt than their counterparts from woodland populations away from roads. While this pattern is consistent with local maladaptation, unresolved insights into the timing and duration of these effects leave open the possibility that negative outcomes are countered during development. Here, we asked whether the survival disadvantage of roadside wood frogs is stage-specific, and whether this disadvantage reverses before metamorphosis. We used a common garden road salt exposure experiment and a field-based reciprocal transplant experiment to examine differences in survival across life-history stage and with respect to population type. In each experimental context, roadside embryos showed a survival disadvantage relative to woodland embryos, and this disadvantage was not reversed prior to metamorphosis. We also found that salt exposure delayed metamorphosis more strongly for roadside than woodland populations. Together, these results suggest that local maladaptation in aquatic-stage wood frogs is driven by embryonic sensitivity to salt and that roadside populations are further compromised by delayed developmental rates. Future studies should consider which embryonic traits fail to adapt to salt toxicity, and how those traits might correlate with terrestrial trait variation.

Local maladaptation of the anther-smut fungus parasitizing Dianthus carthusianorum

Pathogens are generally expected to evolve faster than their hosts and are therefore likely to be locally adapted. However, some pathogens might lag behind in the co-evolutionary arms race because they do not have some of the advantages shared by most other pathogens (e.g., high mutation or recombination rates, short generation time, high dispersal ability). This is the case of Microbotryum fungi that cause the anther smut disease in plants of the family Caryophyllaceae. We investigated the patterns of local adaptation and maladaptation in Microbotryum carthusianorum and its host plant Dianthus carthusianorum. We performed a full cross-inoculation experiment using half-sib plant families and fungal samples originating from three naturally infected populations in the Czech Republic. We specifically asked, which components of pathogen fitness (i.e., infectivity and host manipulation) are affected by local (mal)adaptation. The pathogen was on average 1.6 times more successful in infecting plants from foreign populations compared to plants from its home population. Once the infection was successful, the pathogen accelerated the plant’s flowering and thus increased the opportunity for transmission to new hosts. However, the level of manipulation of host flowering did not differ between home and foreign populations. This study showed that the pathogen’s infectivity followed a clear pattern of local maladaptation, whereas the host manipulation did not. Our study taken together with previous studies of a related anther smut species reveals the pervasiveness of local maladaptation in this group of pathogens that arises as the result of their restricted gene flow and reduced recombination rates.

Spatial patterns in phage-Rhizobium coevolutionary interactions across regions of common bean domestication

Bacteriophages play significant roles in the composition, diversity, and evolution of bacterial communities. Despite their importance, it remains unclear how phage diversity and phage-host interactions are spatially structured. Local adaptation may play a key role. Nitrogen-fixing symbiotic bacteria, known as rhizobia, have been shown to locally adapt to domesticated common bean at its Mesoamerican and Andean sites of origin. This may affect phage-rhizobium interactions. However, knowledge about the diversity and coevolution of phages with their respective Rhizobium populations is lacking. Here, through the study of four phage-Rhizobium communities in Mexico and Argentina, we show that both phage and host diversity is spatially structured. Cross-infection experiments demonstrated that phage infection rates were higher overall in sympatric rhizobia than in allopatric rhizobia except for one Argentinean community, indicating phage local adaptation and host maladaptation. Phage-host interactions were shaped by the genetic identity and geographic origin of both the phage and the host. The phages ranged from specialists to generalists, revealing a nested network of interactions. Our results suggest a key role of local adaptation to resident host bacterial communities in shaping the phage genetic and phenotypic composition, following a similar spatial pattern of diversity and coevolution to that in the host.

Can long‐lived species keep pace with climate change? Evidence of local persistence potential in a widespread conifer

AbstractAimClimate change poses significant challenges for tree species, which are slow to adapt and migrate. Insight into genetic and phenotypic variation under current landscape conditions can be used to gauge persistence potential to future conditions and determine conservation priorities, but landscape effects have been minimally tested in trees. Here, we use Pinus contorta, one of the most widely distributed conifers in North America, to evaluate the influence of landscape heterogeneity on genetic structure as well as the magnitude of local adaptation versus phenotypic plasticity in a widespread tree species.LocationWestern North America.MethodsWe paired landscape genetics with fully reciprocal in situ common gardens to evaluate landscape influence on neutral and adaptive variation across all subspecies of P. contorta.ResultsLandscape barriers alone play a minor role in limiting gene flow, creating marginal geographically‐based structure. Local climate determines population performance, with survival highest at home but growth greatest in mild climates (e.g., warm, wet). Survival of two of the three populations tested was consistent with patterns of local adaptation documented for P. contorta, while growth was indicative of plasticity for populations grown under novel conditions and suggesting that some populations are not currently occupying their climatic optimum.Main ConclusionsOur findings provide insight into the role of the landscape in shaping population genetic structure in a widespread tree species as well as the potential response of local populations to novel conditions, knowledge critical to understanding how widely distributed species may respond to climate change. Geographically based genetic structure and reduced survival under water‐limited conditions may make some populations of widespread tree species more vulnerable to local maladaptation and extirpation. However, genetically diverse and phenotypically plastic populations of widespread trees, such as many of the P. contorta populations sampled and tested here, likely possess high persistence potential.

Genomic Prediction of (Mal)Adaptation Across Current and Future Climatic Landscapes

Signals of local adaptation have been found in many plants and animals, highlighting the heterogeneity in the distribution of adaptive genetic variation throughout species ranges. In the coming decades, global climate change is expected to induce shifts in the selective pressures that shape this adaptive variation. These changes in selective pressures will likely result in varying degrees of local climate maladaptation and spatial reshuffling of the underlying distributions of adaptive alleles. There is a growing interest in using population genomic data to help predict future disruptions to locally adaptive gene-environment associations. One motivation behind such work is to better understand how the effects of changing climate on populations’ short-term fitness could vary spatially across species ranges. Here we review the current use of genomic data to predict the disruption of local adaptation across current and future climates. After assessing goals and motivationsunderlying the approach, we review the main steps and associated statistical methods currently in use and explore our current understanding of the limits and future potential of using genomics to predict climate change (mal)adaptation.

Experimental (co)evolution in a multi‐species microbial community results in local maladaptation

Interspecific coevolutionary interactions can result in rapid biotic adaptation, but most studies have focused only on species pairs. Here, we (co)evolved five microbial species in replicate polycultures and monocultures and quantified local adaptation. Specifically, growth rate assays were used to determine adaptations of each species' populations to (1) the presence of the other four species in general and (2) sympatric vs. allopatric communities. We found that species did not show an increase in net biotic adaptation:ancestral, polyculture- and monoculture-evolved populations did not have significantly different growth rates within communities. However, 4/5 species' growth rates were significantly lower within the community they evolved in relative to an allopatric community. 'Local maladaptation' suggests that species evolved increased competitive interactions to sympatric species' populations. This increased competition did not affect community stability or productivity. Our results suggest that (co)evolution within communities can increase competitive interactions that are specific to (co)evolved community members.

Experimental (co)evolution in a multi-species microbial community results in local maladaptation

Experimental (co)evolution in a multi-species microbial community results in local maladaptation

Evidence for plasticity, but not local adaptation, in invasive Japanese knotweed (Reynoutria japonica) in North America

While local adaptation and phenotypic plasticity are commonly observed in species occupying heterogeneous environments, these phenomena are less well understood in invasive species. However, plant invasions offer the opportunity to study these dynamics as they occur in species colonizing new habitats. In this study, we examined local adaptation and phenotypic plasticity in an invasive plant, Reynoutria japonica, across a broad latitudinal range within North America. We performed full-factorial reciprocal transplants using plants from three sites and examined fitness responses in both sexual and clonal reproductive measures, as well as vegetative responses in height, basal stem diameter, and biomass. For all vegetative traits, there was a significant effect of source population, indicating genetic differentiation among populations. There was also a significant effect of transplant site, suggesting phenotypic plasticity. However, there was no evidence of local adaptation at the North American meta-population level for either measure of sexual or clonal fitness. All three comparisons for sexual fitness failed to show any differences between source populations, indicating a lack of local adaptation. For clonal fitness, two of the three comparisons showed local maladaptation, and only one showed greater fitness at the home compared to foreign sites, but this population had greater fitness at all sites, indicating greater fitness overall for this population rather than local adaptation. The fact that we did not detect consistent patterns of local adaptation in these populations across a broad geographic range is somewhat surprising given that local adaptation appears common in many species, including invasives, and that the populations have been established for over a century. However, the lack of local adaptation observed in this species may indicate that phenotypic plasticity within the species is sufficient to allow the persistence of R. japonica in a variety of environments across its invaded range.

Comparing the consequences of natural selection, adaptive phenotypic plasticity, and matching habitat choice for phenotype-environment matching, population genetic structure, and reproductive isolation in meta-populations.

Organisms commonly experience significant spatiotemporal variation in their environments. In response to such heterogeneity, different mechanisms may act that enhance ecological performance locally. However, depending on the nature of the mechanism involved, the consequences for populations may differ greatly. Building on a previous model that investigated the conditions under which different adaptive mechanisms (co)evolve, this study compares the ecological and evolutionary population consequences of three very different responses to environmental heterogeneity: matching habitat choice (directed gene flow), adaptive plasticity (associated with random gene flow), and divergent natural selection. Using individual‐based simulations, we show that matching habitat choice can have a greater adaptive potential than plasticity or natural selection: it allows for local adaptation while protecting genetic polymorphism despite global mating or strong environmental changes. Our simulations further reveal that increasing environmental fluctuations and unpredictability generally favor the emergence of specialist genotypes but that matching habitat choice is better at preventing local maladaptation by individuals. This confirms that matching habitat choice can speed up the genetic divergence among populations, cause indirect assortative mating via spatial clustering, and hence even facilitate sympatric speciation. This study highlights the potential importance of directed dispersal in local adaptation and speciation, stresses the difficulty of deriving its operation from nonexperimental observational data alone, and helps define a set of ecological conditions which should favor its emergence and subsequent detection in nature.

Galba truncatula and Fasciola hepatica: Genetic costructures and interactions with intermediate host dispersal

Antagonistic interactions between hosts and parasites are key structuring forces in natural populations. Demographic factors like extinction, migration and the effective population size shape host-parasite metapopulational dynamics. Therefore, to understand the evolution of host-parasite systems it is necessary to study the distribution of the genetic variation of both entities simultaneously. In this paper, we investigate the population genetics co-structure of parasites and hosts within a metapopulation of the liver fluke, Fasciola hepatica, and two of its intermediate hosts, the main intermediate host in Europe, Galba truncatula, and a new intermediate host, Omphiscola glabra, in Central France. Our results reveal an absence of specificity of flukes as regard to the two alternative hosts though O. glabra shows higher prevalence of F. hepatica. Host and parasites displayed contrasting population genetics structure with very small, highly inbred (selfing) and strongly isolated G. truncatula populations and much bigger, panmictic and more dispersive F. hepatica. This could indicate a local adaptation of the parasite and a local maladaptation of the host. We also unveil a parasite-mediated biased population genetics structure suggesting that infected G. truncatula disperse more; have higher dispersal survival than uninfected snails or, more likely, that immigrant snails are infected more often than local snails (local parasites are less adapted to local hosts). Finally, an absence, or at least an ambiguous signature of isolation by distance was observed in both host and parasite population. A very weak migration rate for G. truncatula provides a reasonable explanation for this ambiguous result. Alternatively, smaller sample sizes combined with modest migration rates might explain the difficulties to unveil the signal in F. hepatica.

Positive Sire Effects and Adaptive Genotype by Environment Interaction Occur despite Pattern of Local Maladaptation in Roadside Populations of an Amphibian

The global road network causes many negative ecological effects. Contrasting our knowledge of these effects, insights into evolutionary consequences of roads remain undeveloped. Here, we study a suite of populations of the Wood Frog that appear to be evolving maladaptively in response to road-adjacency. Specifically, when raised together in roadside pools, roadside populations survive at lower rates compared to populations away from roads. To begin to understand the cause of this survival disadvantage, we investigated potential parental and genetic sources of maladaptation. First, to assess whether parental effects might induce maladaptation, we measured adult body weight to length ratio (‘relative weight') and its influence on offspring survival in a reciprocal transplant experiment across 12 populations. Next, to assess whether genetic effects might limit adaptive responses in offspring, we estimated genetic correlations between environments for survival and fitness-related traits. We found that relativ...