Molecular Ecology (2009) 18, 1678–1691 doi: 10.1111/j.1365-294X.2009.04142.x
© 2009 Blackwell Publishing Ltd
Blackwell Publishing Ltd
Natural selection influences AFLP intraspecific genetic
variability and introgression patterns in Atlantic eels
P. A. GAGNAIRE,* V. ALBERT,† B. JÓNSSON‡ and L. BERNATCHEZ†
*Institut des Sciences de l’Evolution (ISEM UMR 5554 CNRS-UMII), Université de Montpellier II, CC 065, Place E. Bataillon,
34095 Montpellier cedex 5, France, †Institut de Biologie Intégrative et des Systèmes (IBIS), Université Laval, Québec, Canada G1V 0A6,
‡Institute of Freshwater Fisheries, Northern Division, Sau∂árkrókur, Iceland, IS 550
Abstract
Investigating patterns of genetic variation in hybridizing species provides an opportunity
to understand the impact of natural selection on intraspecific genetic variability and inter-
specific gene exchange. The Atlantic eels Anguilla rostrata and A. anguilla each occupy a
large heterogeneous habitat upon which natural selection could differentially shape
genetic variation. They also produce viable hybrids only found in Iceland. However, the
possible footprint of natural selection on patterns of genetic variation within species and
introgressive hybridization in Icelandic eels has never been assessed. We revisited amplified
fragment length polymorphism data collected previously using population genomics
and admixture analyses to test if (i) genetic variation could be influenced by non-neutral
mechanisms at both the intra- and interspecific levels, and if (ii) selection could shape
the spatio-temporal distribution of Icelandic hybrids. We first found candidate loci for
directional selection within both species. Spatial distributions of allelic frequencies
displayed by some of these loci were possibly related with the geographical patterns of
life-history traits in A. rostrata, and could have been shaped by natural selection associated
with an environmental gradient along European coasts in A. anguilla. Second, we identified
outlier loci at the interspecific level. Non-neutral introgression was strongly suggested for
some of these loci. We detected a locus at which typical A. rostrata allele hardly crossed the
species genetic barrier, whereas three other loci showed accelerated patterns of introgression
into A. anguilla in Iceland. Moreover, the level of introgression at these three loci increased
from the glass eel to the yellow eel stage, supporting the hypothesis that differential
survival of admixed genotypes partly explains the spatio-temporal pattern of hybrid abund-
ance previously documented in Iceland.
Keywords: AFLP, Anguilla, introgressive hybridization, natural selection, outlier loci, species
genetic barrier
Received 5 November 2008; revision received 5 January 2009; accepted 22 January 2009
Introduction
Discerning the relative influence of neutral vs. selective
processes acting in natural populations is a fundamental
step towards the comprehension of species’ evolution.
Populations living in heterogeneous habitats are likely to
undergo diverse selective constraints that can differentially
shape genetic variation among them, occasionally leading
to reproductive isolation (Mayr 1947). Direct observation
of the genetic effects of natural selection can be conveniently
assessed when adaptive phenotypic traits and genes
underlying these adaptations are known. In most nonmodel
organisms, a priori knowledge concerning the genes
governing adaptive traits is often not available, thus, it
becomes necessary to use indirect methods to identify loci
potentially under selection. Such ‘population genomics’
approaches are based on the principle of screening sufficient
number of molecular markers randomly distributed
across the whole genome in a large number of individuals,
to detect loci whose level of differentiation between popula-
tions exceeds that expected under neutral expectations.
Correspondence: Louis Bernatchez, Fax: 1 418 656 7176;
E-mail: louis.bernatchez@bio.ulaval.ca