Anthropogenic and natural drivers of gene flow in a temperate wild fruit tree: a basis for conservation and breeding programs in apples.

Jeanne Ropars,Alice Feurtey,Uriel Gélin,Tatiana Giraud,Kristine Misvanderbrugge,Pierre Gladieux,Amandine Cornille

doi:10.1111/eva.12250

Abstract

Gene flow is an essential component of population adaptation and species evolution. Understanding of the natural and anthropogenic factors affecting gene flow is also critical for the development of appropriate management, breeding, and conservation programs. Here, we explored the natural and anthropogenic factors impacting crop-to-wild and within wild gene flow in apples in Europe using an unprecedented dense sampling of 1889 wild apple (Malus sylvestris) from European forests and 339 apple cultivars (Malus domestica). We made use of genetic, environmental, and ecological data (microsatellite markers, apple production across landscapes and records of apple flower visitors, respectively). We provide the first evidence that both human activities, through apple production, and human disturbance, through modifications of apple flower visitor diversity, have had a significant impact on crop-to-wild interspecific introgression rates. Our analysis also revealed the impact of previous natural climate change on historical gene flow in the nonintrogressed wild apple M. sylvestris, by identifying five distinct genetic groups in Europe and a north–south gradient of genetic diversity. These findings identify human activities and climate as key drivers of gene flow in a wild temperate fruit tree and provide a practical basis for conservation, agroforestry, and breeding programs for apples in Europe.

Highlights

Over the last century, researchers in evolutionary and applied biology have paid much attention to gene flow, which is considered to play a key role in species persistence, evolution, and diversification
We analyzed the structure of M. sylvestris and identified five distinct clusters within the wild species, and in addition a cluster corresponding to M. domestica (Fig. S2)
The use of K values >6 uncovered no further structure within M. sylvestris, indicating that the M. sylvestris 9 M. domestica hybrids detected at K = 6 were not artifacts due to genetic structure within the wild apple gene pool

Summary

Introduction

Researchers in evolutionary and applied biology have paid much attention to gene flow, which is considered to play a key role in species persistence, evolution, and diversification. One central question concerns the extent to which climate changes and recent global changes due to human disturbances (e.g., land-use management and fragmentation) affect gene flow (Manel and Holderegger 2013) This question must be addressed, to make it possible to forecast the impact of these changes on the evolution of populations and to develop appropriate management, breeding, and conservation programs. Over the last 20 years, an array of methods, including autocorrelation, parentage analyses, and assignment methods, Gene flow drivers in apple has been developed for the identification of natural factors affecting gene flow (Pritchard et al 2000; Manel et al 2003; Smouse and Sork 2004; Storfer et al 2010) Studies based on these methods have identified climate as a key driver of within-species historical gene flow in many temperate species in Europe during the Pleistocene (Hewitt 2004). The determination of genetic diversity, differentiation, and admixture across the geographical range of such scattered species can be a practical basis for sustainable management and conservation programs

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Conclusion