Drivers of adaptive capacity in wild populations: implications for genetic interventions

Abstract

The unprecedented rate of environmental change in the Anthropocene poses evolutionary challenges for wild populations globally. Active human interventions are being increasingly considered to accelerate natural adaptive processes. Evolutionary models can evaluate how species may fare under future climate, elucidate which evolutionary processes are critical to rapid adaptation, and how active interventions may influence fitness trajectories of organisms. Here we use polygenic metapopulation adaptation models to quantify the relative importance (effect sizes) of different eco-evolutionary parameters on the rates of adaptation in wild populations i) without active interventions, and ii) under a subset of active interventions. We demonstrate that genetic diversity (heterozygosity, He), population connectivity and the effect size of additive genetic variance are the primary drivers of natural adaptation rates. We quantify the effect sizes of these parameters on population fitness across three proposed assisted evolution scenarios and identify critical thresholds for intervention effectiveness and implementation. Specifically, the interventions tested here were most effective at low levels of genetic diversity in target populations (He < 0.2) and when timed during a cold-to-warm phase of an ENSO-like oscillation. Beneficial levels of connectivity were highly dependent on desired outcomes for the meta-population. We also present a global meta-analysis of genetic diversity in tropical reef-building corals as a case study of how thresholds derived from evolutionary models can be used to guide decision making by managers. We find genetic diversity to be highly variable by coral taxon and region, highlighting how thresholds from evolutionary models can be used in conjunction with empirical data to assess intervention needs and priorities. Finally, we highlight the critical knowledge and data gaps to produce the next suite of applied models for conservation management decision-support.

Semipermeable species boundaries create opportunities for gene flow and adaptive potential

“…The longer term adaptive potential of the hybrids in a changing environment is further supported by our finding of more heterozygosity in hybrids compared to the nonadmixed individuals. Genetic diversity arising from hybridisation may fuel adaptation (Torda & Quigley, 2021) even in the presence of hybrid incompatibilities (Kulmuni et al, 2023) and could provide means to adapt to new environmental challenges (Grant & Grant, 2019; Seehausen, 2013).…”

“…Genetic diversity arising from hybridisation may fuel adaptation (Torda & Quigley, 2021) even in the presence of hybrid incompatibilities (Kulmuni et al, 2023) and could provide means to adapt to new environmental challenges (Grant & Grant, 2019;Seehausen, 2013).…”

“…Hybridisation and gene flow have both positive and negative effects for fitness. Complete reproductive isolation is not necessarily optimal (Barton, 2020): increased genetic diversity through hybridisation may fuel adaptation (Kulmuni et al, 2023; Torda & Quigley, 2021), and introgression has repeatedly underlied adaptation into new niches (De‐Kayne et al, 2022; Kagawa & Takimoto, 2018; Meier et al, 2017). However, populations can also suffer from hybridisation due to deleterious fitness effects (Ålund et al, 2013) and mortality (Ellison et al, 2008), arising from the inviability of offspring or hybrid breakdown in later generations.…”

A roadmap to integrating resilience into the practice of coral reef restoration

“…To integrate diversity at the genetic level into restoration projects, corals should be sourced from a variety of habitats with diverse environmental conditions within species boundaries in the restoration region (Table 1). In less genotypically diverse habitats, practitioners should source corals of the same species from different populations to capture a range of phenotypic traits and genotypes, as genetic diversity can be highly variable across coral species and reef habitats (Shearer et al, 2009; Torda & Quigley, 2021). Current research using four Caribbean coral species suggests that collecting coral fragments from 10 to 35 genetically distinct donor colonies (i.e., “genets”) should capture the majority (50%–95%) of genetic diversity within a species (Shearer et al, 2009).…”