Environmental variation and biotic interactions limit adaptation at ecological margins: lessons from rainforestDrosophilaand European butterflies

Abstract

Models of local adaptation to spatially varying selection predict that maximum rates of evolution are determined by the interaction between increased adaptive potential owing to increased genetic variation, and the cost genetic variation brings by reducing population fitness. We discuss existing and new results from our laboratory assays and field transplants of rainforest Drosophila and UK butterflies along environmental gradients, which try to test these predictions in natural populations. Our data suggest that: (i) local adaptation along ecological gradients is not consistently observed in time and space, especially where biotic and abiotic interactions affect both gradient steepness and genetic variation in fitness; (ii) genetic variation in fitness observed in the laboratory is only sometimes visible to selection in the field, suggesting that demographic costs can remain high without increasing adaptive potential; and (iii) antagonistic interactions between species reduce local productivity, especially at ecological margins. Such antagonistic interactions steepen gradients and may increase the cost of adaptation by increasing its dimensionality. However, where biotic interactions do evolve, rapid range expansion can follow. Future research should test how the environmental sensitivity of genotypes determines their ecological exposure, and its effects on genetic variation in fitness, to predict the probability of evolutionary rescue at ecological margins. This article is part of the theme issue ‘Species’ ranges in the face of changing environments (Part II)’.

Variation in the strength of selection but no trait divergence between elevational extremes in a tropical rainforestDrosophila

“…Gene flow at this scale (between sites 1-10 km apart) is likely to be high in D. birchii, given the low differentiation observed at microsatellite markers between populations separated by hundreds of kilometres (Schiffer et al, 2007). Spatial variation in selection at such a local scale may therefore be small relative to the effect of gene flow between sites, particularly where reductions of population density at high and low elevations mean that gene flow is likely to be asymmetrical and therefore have strong swamping effects on local allele frequencies (O'Brien et al, 2017(O'Brien et al, , 2022.…”

Understanding the biology of species' ranges: when and how does evolution change the rules of ecological engagement?

“…Darwin also argued that biotic interactions should increase at low latitudes, with abiotic effects on fitness dominating at higher latitudes, something for which there is now compelling empirical support [ 24 ]. The importance of biotic interactions in determining range limits remains an important theme in both modelling [ 25 ] and empirical [ 15 , 26 ] studies. In addition, adaptive divergence within species that depends on interactions between spatially variable selection and gene flow has become central to explaining range limits, based on insights from models that integrate population genetics with population ecology [ 27 ].…”

“…Even in plants, transplant experiments that use cuttings to estimate fitness across environments within genotypes need complementary tests of pollen or seed movement to reflect how alleles typically move in natural populations, and to incorporate maternal or early-life effects on phenotypes. O'Brien et al [ 26 ] demonstrate that laboratory-measured variation in fitness in Drosophila rarely relates to field performance, particularly when measured along natural ecological gradients that vary in time as well as space. Their studies also highlight how available genetic variation in the field (as well as its fitness consequences) can be highly environment-dependent, and may act in concert with environmental variation to limit local adaptation in space and time.…”

Introduction to the theme issue ‘Species' ranges in the face of changing environments’

“…O'Brien et al . [ 24 ] discuss how ecological constraints imposed by antagonistic biotic interactions can reduce fitness and increase the steepness of environmental gradients, thereby sharpening limits to adaptation at range margins; alternatively, adaptation to new biotic interactions, such as host shifts [ 24 , 25 ], might facilitate rapid range expansion. Biotic interactions can also influence selection at range limits via trade-offs in responses to abiotic and biotic factors, as illustrated by a simple model developed by Alexander et al .…”