Latitudinal variation in climate‐associated genes imperils range edge populations

Abstract

The ecological impacts of increasing global temperatures are evident in most ecosystems on Earth, but our understanding of how climatic variation influences natural selection and adaptive resilience across latitudes remains largely unknown. Latitudinal gradients allow testing general ecosystem‐level theories relevant to climatic adaptation. We assessed differences in adaptive diversity of populations along a latitudinal region spanning highly variable temperate to subtropical climates. We generated and integrated information from environmental mapping, phenotypic variation and genome‐wide data from across the geographical range of the rainbowfish Melanotaenia duboulayi, an emerging aquatic system for studies of climate change. We detected, after controlling for spatial population structure, strong interactions between genotypes and environment associated with variation in stream flow and temperature. Some of these hydroclimate‐associated genes were found to interact within functional protein networks that contain genes of adaptive significance for projected future climates in rainbowfish. Hydroclimatic selection was also associated with variation in phenotypic traits, including traits known to affect fitness of rainbowfish exposed to different flow environments. Consistent with predictions from the “climatic variability hypothesis,” populations exposed to extremes of important environmental variables showed stronger adaptive divergence and less variation in climate‐associated genes compared to populations at the centre of the environmental gradient. Our findings suggest that populations that evolved at environmental range margins and at geographical range edges may be more vulnerable to changing climates, a finding with implications for predicting adaptive resilience and managing biodiversity under climate change.

Fish out of water: Genomic insights into persistence of rainbowfish populations in the desert

“…Rainbowfishes (genus Melanotaenia) are an emerging Australian system to study hydroclimatically driven adaptive evolution (McGuigan et al 2003;Smith et al 2013;Unmack et al 2013;McCairns et al 2016;Gates et al 2017;Brauer et al 2018;Sandoval-Castillo et al 2020;Smith et al 2020). Here, we integrate high-resolution, satellite-derived surface water data with genome-wide variation and eco-evolutionary simulations to examine the dynamics between connectivity, effective population size, and adaptive diversity in an aquatic obligate of the desert, the desert rainbowfish (Melanotaenia splendida tatei).…”

Environmental selection, rather than neutral processes, best explain patterns of diversity in a tropical rainforest fish

“…The association of these signals thus adds an additional layer of support for the influence of local environment on evolutionary trajectories in the Wet Tropics. This level of integration has so far been uncommon in environmental association studies (Smith et al 2020, Carvalho et al 2021), and we would therefore recommend a similar strategy where both genomic and phenotypic data are available to improve inferences about candidate genes and potential biological relevance.…”

“…More recently, experimental assessments of gene expression have detected selection for plasticity of thermal response mechanisms ( M. duboulayi, M. fluviatilis , and M. s. tatei ) (Smith et al 2013, McCairns et al 2016, Sandoval-Castillo et al 2020). Riverscape GEAs have also supported intraspecies ecological divergence related to hydroclimate for M. fluviatilis (Brauer et al 2018) and M. duboulayi (Smith et al 2020), with the latter including evidence of GxPxE links.…”

“…We therefore capitalise on growing knowledge of eco-evolutionary processes in Australian rainbowfishes ( Melanotaenia spp; family Melanotaeniidae) (e.g. McGuigan et al (2003), McGuigan et al (2005), Smith et al (2013), McCairns et al (2016), Gates et al (2017), Brauer et al (2018), Lisney et al (2020), Sandoval-Castillo et al (2020), Smith et al (2020)). In this genus, previous work has indicated not only the likely importance of hydroclimate as a driver of diversity, but the utility of integrative methods for assessing aquatic adaptation.…”

Variation in intraspecific demography drives localised concordance but species-wide discordance in response to past climatic change

“…The degree to which SGV is maintained within species or populations varies substantially across taxa and is influenced by a combination of demographic, ecological and environmental factors. For example, populations occurring at the edge of a species range often have lower connectivity and genetic diversity than their more central counterparts [ 12 ], including reduced diversity in climate-associated genes [ 13 ]. In marginal populations, persistence is driven by the balance of the steepness of the selective environment and the effectiveness of selection relative to genetic drift [ 14 ].…”