Signatures Of Local Adaptation 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.

Local adaptation can cause both peaks and troughs in nucleotide diversity within populations.

The amount of standing variation present within populations is a fundamental quantity of interest in population genetics, commonly represented by calculating the average number of differences between pairs of nucleotide sequences (nucleotide diversity, π). It is well understood that both background and positive selection can cause reductions in nucleotide diversity, but less clear how local adaptation affects it. Depending on the assumptions and parameters, some theoretical studies have emphasized how local adaptation can reduce nucleotide diversity, while others have shown that it can increase it. Here, we explore how local adaptation shapes genome-wide patterns in within-population nucleotide diversity, extending previous work to study the effects of polygenic adaptation, genotypic redundancy, and population structure. We show that local adaptation produces two very different patterns depending on the relative strengths of migration and selection, either markedly decreasing or increasing within-population diversity at linked sites at equilibrium. At low migration, regions of depleted diversity can extend large distances from the causal locus, with substantially more diversity eroded than expected with background selection. With higher migration, peaks occur over much smaller genomic distances but with much larger magnitude changes in diversity. Across spatially extended environmental gradients, both patterns can be found within a single species, with increases in diversity at the center of the range and decreases towards the periphery. Our results demonstrate that there is no universal diagnostic signature of local adaptation based on within-population nucleotide diversity, so it will not be broadly useful for explaining increased FST. However, given that neither background nor positive selection inflate diversity, when peaks are found they suggest local adaptation may be acting on a causal allele in the region.

Genetic homogeneity and weak signatures of local adaptation in the marine mussel Mytilus chilensis

The natural populations of the marine mussel Mytilus chilensis and the associated aquaculture industry forms a sensitive social-ecological system that relies on the released propagules for cultivation in the highly heterogeneous environment (temperature, productivity, and salinity) of northern Patagonia (42–44 °S). We assessed spatial genetic structure, signals of local adaptation, and population assignment of M. chilensis analyzing 5963 SNPs from 125 individuals across six natural populations sampled over two consecutive years along the southeast Pacific coast (39° 25′ to 43° 07′ S, ~ 430 km). Neutral and putatively adaptive loci revealed high genetic diversity and low genetic differentiation among populations. Of the whole dataset, less than 1% (50) of loci were identified as putatively adaptive through multiple approaches, with only 0.1% detected in by all of them, and only two loci of them were correlated with environmental variables. No evidence of Isolation by Environment (IBE) was found, albeit a slight differentiation in the southern sampling location (Yaldad). These results suggest that the genetic structure observed is primarily shaped by neutral processes with weak signals of local adaptation. Gene-flow appears to be the main evolutionary force influencing the species’ population genetic structure. Because of the importance for the industry, the probability of correct assignment of individuals to their population of origin using allelic frequencies was evaluated. Analyses exhibited relatively low probabilities (< 50% for four out of six sites) of accurately assigning individuals to their geographic origin, with a limited success of SNP markers the for such purposes. Likely, species' high dispersal capacity, seed translocation, and the spill-over effect of mussel aquaculture prevents population genetic differentiation through high effective gene flow, hindering local genetic adaptation.

Spatial variation in genomic signatures of local adaptation during the cane toad invasion of Australia.

Adaptive evolution can facilitate species' range expansions across environmentally heterogeneous landscapes. However, serial founder effects can limit the efficacy of selection, and the evolution of increased dispersal during range expansions may result in gene flow swamping local adaptation. Here, we study how genetic drift, gene flow and selection interact during the cane toad's (Rhinella marina) invasion across the heterogeneous landscape of Australia. Following its introduction in 1935, the cane toad colonised eastern Australia and established several stable range edges. The ongoing, more rapid range expansion in north-central Australia has occurred concomitant with an evolved increase in dispersal capacity. Using reduced representation genomic data of Australian cane toads from the expansion front and from two areas of their established range, we test the hypothesis that high gene flow constrains local adaptation at the expansion front relative to established areas. Genetic analyses indicate the three study areas are genetically distinct but show similar levels of allelic richness, heterozygosity and inbreeding. Markedly higher gene flow or recency of colonisation at the expansion front have likely hindered local adaptation at the time of sampling, as indicated by reduced slopes of genetic-environment associations (GEAs) estimated using a novel application of geographically weighted regression that accounts for allele surfing; GEA slopes are significantly steeper in established parts of the range. Our work bolsters evidence supporting adaptation of invasive species post-introduction and adds novel evidence for differing strengths of evolutionary forces among geographic areas with different invasion histories.

Rolling down that mountain: microgeographical adaptive divergence during a fast population expansion along a steep environmental gradient in European beech

Forest tree populations harbour high genetic diversity thanks to large effective population sizes and strong gene flow, allowing them to diversify through adaptation to local environmental pressures within dispersal distance. Many tree populations also experienced historical demographic fluctuations, including spatial population contraction or expansions at various temporal scales, which may constrain their ability to adapt to environmental variations. Our aim is to investigate how recent contraction and expansion events interfere with local adaptation, by studying patterns of adaptive divergence between closely related stands undergoing environmentally contrasted conditions, and having or not recently expanded. To investigate genome-wide signatures of local adaptation while accounting for demography, we analysed divergence in a European beech population by testing pairwise differentiation among four tree stands at ~35k Single Nucleotide Polymorphisms from ~9k genomic regions. We applied three divergence outlier search methods resting on different assumptions and targeting either single SNPs or contiguous genomic regions, while accounting for the effect of population size variations on genetic divergence. We found 27 signals of selective signatures in 19 target regions. Putatively adaptive divergence involved all stand pairs. We retrieved signals both when comparing old-growth stands and recently colonised areas and when comparing stands within the old-growth area. Therefore, adaptive divergence processes have taken place both over short time spans, under strong environmental contrasts, and over short ecological gradients, in populations that have been stable in the long term. This suggests that standing genetic variation supports local, microgeographic divergence processes, which can maintain genetic diversity at the landscape level.

Biotic interactions promote local adaptation to soil in plants

Although different ecological factors shape adaptative evolution in natural habitats, we know little about how their interactions impact local adaptation. Here we used eight generations of experimental evolution with outcrossing Brassica rapa plants as a model system, in eight treatment groups that varied in soil type, herbivory (with/without aphids), and pollination mode (hand- or bumblebee-pollination), to study how biotic interactions affect local adaptation to soil. First, we show that several plant traits evolved in response to biotic interactions in a soil-specific way. Second, using a reciprocal transplant experiment, we demonstrate that significant local adaptation to soil-type evolved in the “number of open flowers”, a trait used as a fitness proxy, but only in plants that evolved with herbivory and bee pollination. Whole genome re-sequencing of experimental lines revealed that biotic interactions caused a 10-fold increase in the number of SNPs across the genome with significant allele frequency change, and that alleles with opposite allele frequency change in different soil types (antagonistic pleiotropy) were most common in plants with an evolutionary history of herbivory and bee pollination. Our results demonstrate that the interaction with mutualists and antagonists can facilitate local adaptation to soil type through antagonistic pleiotropy.

Complex patterns of genetic structure in the sea cucumber Holothuria (Metriatyla) scabra from the Philippines: implications for aquaculture and fishery management

The sandfish Holothuria (Metriatyla) scabra, is a high-value tropical sea cucumber harvested from wild stocks for over four centuries in multi-species fisheries across its Indo-Pacific distribution, for the global bêche-de-mer (BDM) trade. Within Southeast Asia, the Philippines is an important centre of the BDM trade, however overharvesting and largely open fishery management have resulted in declining catch volumes. Sandfish mariculture has been developed to supplement BDM supply and assist restocking efforts; however, it is heavily reliant on wild populations for broodstock supply. Consequently, to inform fishery, mariculture, germplasm and translocation management policies for both wild and captive resources, a high-resolution genomic audit of 16 wild sandfish populations was conducted, employing a proven genotyping-by-sequencing approach for this species (DArTseq). Genomic data (8,266 selectively-neutral and 117 putatively-adaptive SNPs) were used to assess fine-scale genetic structure, diversity, relatedness, population connectivity and local adaptation at both broad (biogeographic region) and local (within-biogeographic region) scales. An independent hydrodynamic particle dispersal model was also used to assess population connectivity. The overall pattern of population differentiation at the country level for H. scabra in the Philippines is complex, with nine genetic stocks and respective management units delineated across 5 biogeographic regions: (1) Celebes Sea, (2) North and (3) South Philippine Seas, (4) South China and Internal Seas and (5) Sulu Sea. Genetic connectivity is highest within proximate marine biogeographic regions (mean Fst=0.016), with greater separation evident between geographically distant sites (Fst range=0.041–0.045). Signatures of local adaptation were detected among six biogeographic regions, with genetic bottlenecks at 5 sites, particularly within historically heavily-exploited locations in the western and central Philippines. Genetic structure is influenced by geographic distance, larval dispersal capacity, species-specific larval development and settlement attributes, variable ocean current-mediated gene flow, source and sink location geography and habitat heterogeneity across the archipelago. Data reported here will inform accurate and sustainable fishery regulation, conservation of genetic diversity, direct broodstock sourcing for mariculture and guide restocking interventions across the Philippines.

Shared xerophytic genes and their re-use in local adaptation to aridity in the desert plant Gymnocarpos przewalskii.

In order to thrive and survive, plant species need to combine stability in the long term and rapid response to environmental challenges in the short term. The former would be reflected by parallel or convergent adaptation across species, and the latter by pronounced local adaptation among populations of the same species. In the present study, we generated a high-quality genome and re-sequenced 177 individuals for Gymnocarpos przewalskii, an important desert plant species from North-West China, to detect local adaptation. We first focus on ancient adaptation to aridity at the molecular level by comparing the genomic data of 15 species that vary in their ability to withstand aridity. We found that a total of 118 genes were shared across xerophytic species but absent from non-xerophytic species. Of the 65 found in G. przewalskii, 63 were under purifying selection and two under positive selection. We then focused on local adaptation. Up to 20% of the G. przewalskii genome showed signatures of local adaptation to aridity during population divergence. Thirteen of the selected shared xerophytic genes were reused in local adaptation after population differentiation. Hence, only about 20% of the genes shared and specific to xerophytic species and associated with adaptation to aridity were later recruited for local adaptation in G. przewalskii.

Signatures of adaptation at key insecticide resistance loci in Anopheles gambiae in Southern Ghana revealed by reduced-coverage WGS

Resistance to insecticides and adaptation to a diverse range of environments present challenges to Anopheles gambiae s.l. mosquito control efforts in sub-Saharan Africa. Whole-genome-sequencing is often employed for identifying the genomic basis underlying adaptation in Anopheles, but remains expensive for large-scale surveys. Reduced coverage whole-genome-sequencing can identify regions of the genome involved in adaptation at a lower cost, but is currently untested in Anopheles mosquitoes. Here, we use reduced coverage WGS to investigate population genetic structure and identify signatures of local adaptation in Anopheles mosquitoes across southern Ghana. In contrast to previous analyses, we find no structuring by ecoregion, with Anopheles coluzzii and Anopheles gambiae populations largely displaying the hallmarks of large, unstructured populations. However, we find signatures of selection at insecticide resistance loci that appear ubiquitous across ecoregions in An. coluzzii, and strongest in forest ecoregions in An. gambiae. Our study highlights resistance candidate genes in this region, and validates reduced coverage WGS, potentially to very low coverage levels, for population genomics and exploratory surveys for adaptation in Anopheles taxa.

The drivers of intraspecific trait variation and their implications for future tree productivity and survival.

Forests are facing unprecedented levels of stress from pest and disease outbreaks, disturbance, fragmentation, development, and a changing climate. These selective agents act to alter forest composition from regional to cellular levels. Thus, a central challenge for understanding how forests will be impacted by future change is how to integrate across scales of biology. Phenotype, or an observable trait, is the product of an individual's genes (G) and the environment in which an organism lives (E). To date, researchers have detailed how environment drives variation in tree phenotypes over long time periods (e.g., long-term ecological research sites [LTERs]) and across large spatial scales (e.g., flux network). In parallel, researchers have discovered the genes and pathways that govern phenotypes, finding high degrees of genetic control and signatures of local adaptation in many plant traits. However, the research in these two areas remain largely independent of each other, hindering our ability to generate accurate predictions of plant response to environment, an increasingly urgent need given threats to forest systems. I present the importance of both genes and environment in determining tree responses to climate stress. I highlight why the difference between G versus E in driving variation is critical for our understanding of climate responses, then propose means of accelerating research that examines G and E simultaneously by leveraging existing long-term, large-scale phenotypic data sets from ecological networks and adding newly affordable sequence (-omics) data to both drill down to find the genes and alleles influencing phenotypes and scale up to find how patterns of demography and local adaptation may influence future response to change.

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.

Mosaic of local adaptation between white clover and rhizobia along an urbanization gradient

Abstract Urbanization frequently alters the biotic and abiotic environmental context. Variation in both the biotic and abiotic environment can result in selection mosaics that lead to locally adapted phenotypes. Ecological changes to urban environments can result in evolutionary responses across a diverse array of plants and animals, but the effects of urbanization on local adaptation and coevolution between species remain largely unstudied. Using a common garden experiment of 30 populations and 1080 plants, we tested for local adaptation in the mutualism between white clover (Trifolium repens) and rhizobia (Rhizobium leguminosarum symbiovar trifolii) along an urbanization gradient. We asked: (Q1) are white clover and rhizobia locally adapted? (Q2) Does nitrogen (N) addition mediate the strength of local adaptation? (Q3) Is the strength of local adaptation in host plants related to the strength of local adaptation in rhizobia, as expected if white clover and rhizobia are coadapting? And (Q4) how does the degree of local adaptation vary with urbanization? We found evidence for local adaptation for both white clover and rhizobia, with stronger signatures of local adaptation for rhizobia than white clover (Q1). While N addition positively affected plant biomass and negatively affected nodule density, N addition did not consistently mediate patterns of local adaptation (Q2). The strength of local adaptation was positively related between white clover and rhizobia under N addition, suggesting that soil N mediates coadaptation between white clover and rhizobia (Q3). We did not find a consistent relationship between measures of urbanization and local adaptation (Q4). Additionally, fitness responses for white clover and rhizobia were unrelated to Rhizobium abundance and local adaptation was unrelated to the broader bacterial microbiome in the soil inoculants or root endosphere. Synthesis. Our results show a spatial mosaic in local adaptation, with stronger local adaptation for rhizobia than white clover. While urbanization does influence the ecology of plant–microbe interactions, our study suggests urbanization does not disrupt local adaptation and coevolution among mutualists.

Genomic responses to climate: Understanding local adaptation in the Andean tree species Nothofagus pumilio and implications for a changing world

Societal Impact StatementForest trees tend to be strongly genetically adapted to their local environments, but climate change will probably subject trees to novel combinations of precipitation, temperature, and photoperiod. Local adaptation was investigated in the ecologically and economically important Patagonian tree species Nothofagus pumilio by characterizing its genetic diversity in relation to the varied environmental conditions across its range. These insights are useful for conservation and management decisions, for example by identifying suitable populations to establish seed source plantations for restoration and characterizing relationships with environmental drivers of selection to better understand how this species will respond to climate change.SummaryNothofagus pumilio is a foundation tree species that inhabits a 2000‐km‐long range in the southern Andes, a region with two perpendicular environmental gradients: temperature and photoperiod (North–South), and precipitation (West–East). We investigated local adaptation patterns by searching for relationships between environmental clines and signatures of adaptation in candidate genes related to stress response, growth, and phenology. Using a paired site sampling design within a landscape genome analysis, we analyzed 493 adult N. pumilio trees in 20 sampling sites across the species' latitudinal range. We screened 47,336 single nucleotide polymorphism (SNP) loci in 1632 contigs (i.e., coding regions along the genome). Population structure and genetic diversity analyses preceded four genome scan analyses using genetic and environmental data. Population structure and genetic diversity are mainly oriented along the latitude axis. Genome scans identified 445 outlier SNPs, which are loci showing signatures of selection. Temperature and photoperiod variables were associated with notably more outliers than precipitation. However, the most frequent biological functions among genes were water deprivation response and cold response, suggesting that stress response is comprised of complex and polygenic traits that are affected by many environmental variables. Our findings suggest that N. pumilio shows signatures of local adaptation to extant climate conditions, including temperature, photoperiod, and precipitation. However, climate change is likely to alter existing relationships among environmental conditions to which this species is currently adapted. These changes may have unpredictable consequences for the species' future survival, adaptation potential, and the people who depend upon these forests.

Signatures of local adaptation to current and future climate in phenology-related genes in natural populations of Quercus robur

BackgroundLocal adaptation is a key evolutionary process that enhances the growth of plants in their native habitat compared to non-native habitats, resulting in patterns of adaptive genetic variation across the entire geographic range of the species. The study of population adaptation to local environments and predicting their response to future climate change is important because of climate change.ResultsHere, we explored the genetic diversity of candidate genes associated with bud burst in pedunculate oak individuals sampled from 6 populations in Poland. Single nucleotide polymorphism (SNP) diversity was assessed in 720 candidate genes using the sequence capture technique, yielding 18,799 SNPs. Using landscape genomic approaches, we identified 8 FST outliers and 781 unique SNPs in 389 genes associated with geography, climate, and phenotypic variables (individual/family spring and autumn phenology, family diameter at breast height (DBH), height, and survival) that are potentially involved in local adaptation. Then, using a nonlinear multivariate model, Gradient Forests, we identified vulnerable areas of the pedunculate oak distribution in Poland that are at risk from climate change.ConclusionsThe model revealed that pedunculate oak populations in the eastern part of the analyzed geographical region are the most sensitive to climate change. Our results might offer an initial evaluation of a potential management strategy for preserving the genetic diversity of pedunculate oak.

Divergent gametic thermal performance and floral warming across an elevation gradient.

Thermal environments vary widely across species ranges, establishing the potential for local adaptation of thermal performance optima and tolerance. In the absence of local adaptation, selection should favor mechanisms to meet thermal optima. Floral temperature is a major determinant of reproductive success in angiosperms, yet whether gametic thermal performance shows signatures of local adaptation across temperature gradients, and how variation in gametic thermal performance influences floral evolution, is unknown. We characterized flowering season temperatures for the forb, Argentina anserina, at extremes of a 1000 m elevation gradient and generated thermal performance curves for pollen and ovule performance in populations at each extreme. Thermal optima fell between mean and maximum intrafloral temperatures. However, cooler high-elevation populations had ~4 °C greater pollen thermal optima than warmer low-elevation populations, while tolerance breadths did not differ. We then tested whether plants at elevational extremes differentially warmed the floral microenvironment. High-elevation flowers warmed significantly more than low, bringing intrafloral temperatures nearer the pollen optima. A manipulative experiment demonstrated that stronger warming in high elevation was conferred by floral tissues. Elevational divergence in floral warming may be driven, in part, by selection on flowers to meet different thermal demands of the gametophytes.

Parallel shifts in flight-height associated with altitude across incipient Heliconius species.

Vertical gradients in microclimate, resource availability, and interspecific interactions are thought to underly stratification patterns in tropical insect communities. However, only a few studies have explored the adaptive significance of vertical space use during the early stages of reproductive isolation. We analysed flight-height variation across speciation events in Heliconius butterflies, representing parallel colonizations of high-altitude forest. We measured flight-height in wild H. erato venus and H. chestertonii, parapatric lowland and mountain specialists, respectively, and found that H. chestertonii consistently flies at a lower height. By comparing our data to previously published results for the ecologically equivalent H. e. cyrbia (lowland) and H. himera (high altitude), we found that the species flying closest to the ground are those that recently colonized high-altitude forests. We show that these repeated trends largely result from shared patterns of ecological selection producing parallel trait-shifts in H. himera and H. chestertonii. Although our results imply a signature of local adaptation, we did not find an association between resource distribution and flight-height in H. e. venus and H. chestertonii. We discuss how this pattern may be explained by variations in forest structure and microclimate. Overall, our findings underscore the importance of behavioural adjustments during early divergence mediated by altitude-shifts.

Divergent selection in a Mediterranean pine on local spatial scales

Abstract The effects of selection on an organism's genome are hard to detect on small spatial scales, as gene flow can swamp signatures of local adaptation. Therefore, most genome scans to detect signatures of environmental selection are performed on large spatial scales; however, divergent selection on the local scale (e.g. between contrasting soil conditions) has also been demonstrated, in particular for herbaceous plants. Here, we hypothesised that in topographically complex landscapes, microenvironment variability is strong enough to leave a selective footprint in the genomes of long‐lived organisms. To test this, we investigated paired south‐ versus north‐facing Pinus pinaster stands on the local scale, with trees growing in close vicinity (≤820 m distance between paired south‐ and north‐facing stands), in a Mediterranean mountain area. While trees on north‐facing slopes experience less radiation, trees on south‐facing slopes suffer from especially harsh conditions, particularly during the dry summer season. Two outlier analyses consistently revealed five putatively adaptive loci (out of 4034), in candidate genes two of which encoded non‐synonymous substitutions. Additionally, one locus showed consistent allele frequency differences in all three stand pairs indicating divergent selection despite high gene flow on the local scale. Permutation tests demonstrated that our findings were robust. Functional annotation of these candidate genes revealed biological functions related to abiotic stress response, such as water availability, in other plant species. Synthesis. Our study highlights how divergent selection in heterogeneous microenvironments shapes and maintains the functional genetic variation within populations of long‐lived forest tree species, being the first to focus on adaptive genetic divergence between south‐ and north‐facing slopes within continuous forest stands. This is especially relevant in the current context of climate change, as this variation is at the base of plant population responses to future climate.

Genetic architecture of the response of Arabidopsis thaliana to a native plant-growth-promoting bacterial strain.

By improving plant nutrition and alleviating abiotic and biotic stresses, plant growth-promoting bacteria (PGPB) can help to develop eco-friendly and sustainable agricultural practices. Besides climatic conditions, soil conditions, and microbe-microbe interactions, the host genotype influences the effectiveness of PGPB. Yet, most GWAS conducted to characterize the genetic architecture of response to PGPB are based on non-native interactions between a host plant and PGPB strains isolated from the belowground compartment of other plants. In this study, a GWAS was set up under in vitro conditions to describe the genetic architecture of the response of Arabidopsis thaliana to the PGPB Pseudomonas siliginis, by inoculating seeds of 162 natural accessions from the southwest of France with one strain isolated from the leaf compartment in the same geographical region. Strong genetic variation of plant growth response to this native PGPB was observed at a regional scale, with the strain having a positive effect on the vegetative growth of small plants and a negative effect on the vegetative growth of large plants. The polygenic genetic architecture underlying this negative trade-off showed suggestive signatures of local adaptation. The main eco-evolutionary relevant candidate genes are involved in seed and root development.

Genomic signals of local adaptation across climatically heterogenous habitats in an invasive tropical fruit fly (Bactrocera tryoni)

Local adaptation plays a key role in the successful establishment of pest populations in new environments by enabling them to tolerate novel biotic and abiotic conditions experienced outside their native range. However, the genomic underpinnings of such adaptive responses remain unclear, especially for agriculturally important pests. We investigated population genomic signatures in the tropical/subtropical Queensland fruit fly, Bactrocera tryoni, which has an expanded range encompassing temperate and arid zones in Australia, and tropical zones in the Pacific Islands. Using reduced representation sequencing data from 28 populations, we detected allele frequency shifts associated with the native/invasive status of populations and identified environmental factors that have likely driven population differentiation. We also determined that precipitation, temperature, and geographic variables explain allelic shifts across the distribution range of B. tryoni. We found spatial heterogeneity in signatures of local adaptation across various climatic conditions in invaded areas. Specifically, disjunct invasive populations in the tropical Pacific Islands and arid zones of Australia were characterised by multiple significantly differentiated single nucleotide polymorphisms (SNPs), some of which were associated with genes with well-understood function in environmental stress (e.g., heat and desiccation) response. However, invasive populations in southeast Australian temperate zones showed higher gene flow with the native range and lacked a strong local adaptive signal. These results suggest that population connectivity with the native range has differentially affected local adaptive patterns in different invasive populations. Overall, our findings provide insights into the evolutionary underpinnings of invasion success of an important horticultural pest in climatically distinct environments.

Heritable variation in thermal profiles is associated with reproductive success in the world's largest bird.

Organisms inhabiting extreme thermal environments, such as desert birds, have evolved spectacular adaptations to thermoregulate during hot and cold conditions. However, our knowledge of selection for thermoregulation and the potential for evolutionary responses is limited, particularly for large organisms experiencing extreme temperature fluctuations. Here we use thermal imaging to quantify selection and genetic variation in thermoregulation in ostriches (Struthio camelus), the world's largest bird species that is experiencing increasingly volatile temperatures. We found that females who are better at regulating their head temperatures ("thermoregulatory capacity") had higher egg-laying rates under hotter conditions. Thermoregulatory capacity was both heritable and showed signatures of local adaptation: females originating from more unpredictable climates were better at regulating their head temperatures in response to temperature fluctuations. Together these results reveal that past and present evolutionary processes have shaped genetic variation in thermoregulatory capacity, which appears to protect critical organs, such as the brain, from extreme temperatures during reproduction.