Identifying targets and agents of selection: innovative methods to evaluate the processes that contribute to local adaptation

Abstract

Summary Extensive empirical work has demonstrated local adaptation to discrete environments, yet few studies have elucidated the genetic and environment mechanisms that generate it. Here, we advocate for research that broadens our understanding of local adaptation beyond pattern and towards process. We discuss how studies of local adaptation can be designed to address two unresolved questions in evolutionary ecology: Does local adaptation result from fitness trade‐offs at individual loci across habitats? How do agents of selection interact to generate local adaptation to discrete contrasting habitats types and continuous environmental gradients? To inform future investigations of the genetic basis of local adaptation, we conducted a literature review of studies that mapped quantitative trait loci (QTL) for fitness in native field environments using reciprocal transplant experiments with hybrid mapping populations or Genome‐wide Association Study (GWAS) panels. We then reviewed the literature for field experiments that disentangle the contributions of various agents of selection to local adaptation. For each question, we suggest future lines of inquiry and discuss implications for climate change and agriculture research. (i) Studies in the native habitats of five biological systems revealed that local adaptation is more often caused by conditional neutrality than genetic trade‐offs at the level of the QTL. We consider the ramifications of this result and discuss knowledge gaps in our current understanding of the genetic basis of local adaptation. (ii) We uncovered only five studies that identified the agents of selection that contribute to local adaptation, and nearly all were conducted in discrete habitats rather than across the continuous environmental gradients that many species inhabit. We introduce a novel experimental framework for illuminating the processes underlying local adaptation. A holistic view of local adaptation is critical for predicting the responses of organisms to climate change, enhancing conservation efforts, and developing strategies to improve crop resilience to environmental stress. Experiments that manipulate agents of selection in native field environments using pedigreed populations or GWAS panels offer unique opportunities for detecting the genetic and environmental mechanisms that generate local adaptation.

Gene regulatory divergence between locally adapted ecotypes in their native habitats

“…Theoretical models (Dieckmann & Doebeli, ; Hedrick, ; Hedrick, Ginevan, & Ewing, ; Levene, ) and studies in key model systems (Abzhanov, Protas, Grant, Grant, & Tabin, ; Barrett, Rogers, & Schluter, ; Hoekstra et al., ) have suggested trade‐offs at individual loci (e.g., antagonistic pleiotropy) to be common. However, field reciprocal transplant experiments and experimental evolution studies have often found a pattern of conditional neutrality, where loci have a strong effect on fitness in one environment but have an undetectable effect on fitness in alternative environments (reviewed in Bono, Smith, Pfennig, & Burch, ; Wadgymar et al., ). This pattern has also been found in the coastal perennial/inland annual M. guttatus system, where three salt tolerance QTLs have fitness effects in coastal habitat but no detectable effects in inland habitat (Lowry et al., ).…”

“…One of the most important forces driving the evolution of ecological specialization and the origin of biodiversity is local adaptation (Clausen, ; Colosimo et al., ; Sobel, Chen, Watt, & Schemske, ). Local adaptation is characterized by reciprocal home‐site advantage, whereby populations perform best in their home habitat while performing poorly in foreign habitats (Hereford, ; Hoekstra, Hirschmann, Bundey, Insel, & Crossland, ; Kawecki & Ebert, ; Wadgymar et al., ). Numerous reciprocal transplant experiments have identified locally adapted populations (Leimu & Fischer ; Hereford, ).…”

“…Numerous reciprocal transplant experiments have identified locally adapted populations (Leimu & Fischer ; Hereford, ). Recently, reciprocal transplant experiments have been combined with genetic studies to quantify the role of individual loci in generating adaptive divergence between local populations (Agren, Oakley, McKay, Lovell, & Schemske, ; Anderson, Lee, Rushworth, Colautti, & Mitchell‐Olds, ; Anderson, Willis, & Mitchell‐Olds, ; Gardner & Latta, ; Leinonen, Remington, Leppala, & Savolainen, ; Lowry, Hall, Salt, & Willis, ; Lowry & Willis, ; Verhoeven, Poorter, Nevo, & Biere, ; Wadgymar et al., ). Despite this advance of integrating transplant experiments with modern genetic techniques, we have a very limited understanding of how gene expression divergence manifests between locally adapted populations in nature.…”

Resource availability alters fitness trade‐offs: implications for evolution in stressful environments

“…Variation in climatic, edaphic, and abiotic agents of selection across space can favor the evolution of local adaptation, such that ecotypes have enhanced performance in their home sites and reduced fitness in contrasting environments (Kawecki and Ebert, 2004). Disentangling the causal agents of local adaptation remains challenging because multiple interacting factors can contribute to fitness trade-offs across environments (Lowry et al, 2008;Wadgymar et al, 2017b). In some systems, variation in climatic factors has been directly linked to local adaptation (Liancourt et al, 2013;Anderson and Wadgymar, 2020).…”

Evolutionary and ecological functional genomics, from lab to the wild

“…Studies have been able to leverage ‘omics’ technologies in the field to study the basis of local adaptation (Knight et al ., ; Gould et al ., ) and contribute to the understanding of changing environmental conditions and climate change (Fournier‐Level et al ., ; Hancock et al ., ; Nagano et al ., ; Plessis et al ., ; D'Agui et al ., ). Experiments that manipulate agents of selection in native field environments using pedigreed populations or GWAS panels also offer unique opportunities for detecting the genetic and environmental mechanisms that generate local adaptation (Wadgymar et al ., ). Combinatorial, multi‐location experimental set‐ups and reciprocal transplant experiments can unlock fitness‐associated loci relative to climate, macro‐ and microbiota, and local adaptation (Wilczek et al ., ; Fournier‐Level et al ., ; Agrawal et al ., ; Prasad et al ., ; Züst et al ., ; Wagner et al ., ; Brachi et al ., ).…”