TY - JOUR

T1 - Population-Specific Selection on Standing Variation Generated by Lateral Gene Transfers in a Grass

AU - Olofsson, Jill K.

AU - Dunning, Luke T.

AU - Lundgren, Marjorie R.

AU - Barton, Henry J.

AU - Thompson, John

AU - Cuff, Nicholas

AU - Ariyarathne, Menaka

AU - Yakandawala, Deepthi

AU - Sotelo, Graciela

AU - Zeng, Kai

AU - Osborne, Colin P.

AU - Nosil, Patrik

AU - Christin, Pascal-Antoine

N1 - Copyright © 2019 The Author(s). Published by Elsevier Ltd.. All rights reserved.

PY - 2019

Y1 - 2019

N2 - Evidence of eukaryote-to-eukaryote lateral gene transfer (LGT) has accumulated in recent years [1-14], but the selective pressures governing the evolutionary fate of these genes within recipient species remain largely unexplored [15, 16]. Among non-parasitic plants, successful LGT has been reported between different grass species [5, 8, 11, 16-19]. Here, we use the grass Alloteropsis semialata, a species that possesses multigene LGT fragments that were acquired recently from distantly related grass species [5, 11, 16], to test the hypothesis that the successful LGT conferred an advantage and were thus rapidly swept into the recipient species. Combining whole-genome and population-level RAD sequencing, we show that the multigene LGT fragments were rapidly integrated in the recipient genome, likely due to positive selection for genes encoding proteins that added novel functions. These fragments also contained physically linked hitchhiking protein-coding genes, and subsequent genomic erosion has generated gene presence-absence polymorphisms that persist in multiple geographic locations, becoming part of the standing genetic variation. Importantly, one of the hitchhiking genes underwent a secondary rapid spread in some populations. This shows that eukaryotic LGT can have a delayed impact, contributing to local adaptation and intraspecific ecological diversification. Therefore, while short-term LGT integration is mediated by positive selection on some of the transferred genes, physically linked hitchhikers can remain functional and augment the standing genetic variation with delayed adaptive consequences.

AB - Evidence of eukaryote-to-eukaryote lateral gene transfer (LGT) has accumulated in recent years [1-14], but the selective pressures governing the evolutionary fate of these genes within recipient species remain largely unexplored [15, 16]. Among non-parasitic plants, successful LGT has been reported between different grass species [5, 8, 11, 16-19]. Here, we use the grass Alloteropsis semialata, a species that possesses multigene LGT fragments that were acquired recently from distantly related grass species [5, 11, 16], to test the hypothesis that the successful LGT conferred an advantage and were thus rapidly swept into the recipient species. Combining whole-genome and population-level RAD sequencing, we show that the multigene LGT fragments were rapidly integrated in the recipient genome, likely due to positive selection for genes encoding proteins that added novel functions. These fragments also contained physically linked hitchhiking protein-coding genes, and subsequent genomic erosion has generated gene presence-absence polymorphisms that persist in multiple geographic locations, becoming part of the standing genetic variation. Importantly, one of the hitchhiking genes underwent a secondary rapid spread in some populations. This shows that eukaryotic LGT can have a delayed impact, contributing to local adaptation and intraspecific ecological diversification. Therefore, while short-term LGT integration is mediated by positive selection on some of the transferred genes, physically linked hitchhikers can remain functional and augment the standing genetic variation with delayed adaptive consequences.

U2 - 10.1016/j.cub.2019.09.023

DO - 10.1016/j.cub.2019.09.023

M3 - Journal article

C2 - 31679927

VL - 29

SP - 3921-3927, e1-e5

JO - Current Biology

JF - Current Biology

SN - 0960-9822

IS - 22

ER -