Detection of molecular signatures of selection at microsatellite loci in the
South African abalone (Haliotis midae) using a population genomic approach
Clint Rhode ⁎, Jessica Vervalle, Aletta E. Bester-van der Merwe, Rouvay Roodt-Wilding
Department of Genetics, Stellenbosch University, Private Bag X1, Matieland, 7602, South Africa
abstract article info
Article history:
Received 12 July 2012
Received in revised form 12 March 2013
Accepted 17 March 2013
Keywords:
Adaptation
F
st
-outlier
Linkage disequilibrium
Neutrality
Population genomics
Selection
Identifying genomic regions that may be under selection is important for elucidating the genetic architecture
of complex phenotypes underlying adaptation to heterogeneous environments. A population genomic
approach, using a classical neutrality test and various F
st
-outlier detection methods was employed to evaluate
genome-wide polymorphism data in order to identify loci that may be candidates for selection amongst six
populations (three cultured and three wild) of the South African abalone, Haliotis midae. Approximately 9%
of the genome-wide microsatellite markers were putatively subject to directional selection, whilst 6–18%
of the genome is thought to be influenced by balancing selection. Genetic diversity estimates for candidate
loci under directional selection was significantly reduced in comparison to candidate neutral loci, whilst can-
didate balancing selection loci demonstrated significantly higher levels of genetic diversity (Kruskal–Wallis
test, P b 0.05). Pairwise F
st
estimates based on candidate directional selection loci also demonstrated in-
creased levels of differentiation between study populations. Various candidate loci under selection showed
significant inter-chromosomal linkage disequilibrium, suggesting possible gene-networks underling adaptive
phenotypes. Furthermore, several loci had significant hits to known genes when performing BLAST searches
to NCBI's non-redundant databases, whilst others are known to be derived from expressed sequences even
though homology to a known gene could not be established. A number of loci also demonstrated relatively
high similarity to transposable elements. The association of these loci to functional and genomically active
sequences could in part explain the observed signatures of selection.
© 2013 Elsevier B.V. All rights reserved.
1. Introduction
Understanding how selection shapes molecular diversity and how
this diversity in turn facilitates the development of phenotypes, in
heterogeneous environments, has become a key endeavour of modern
evolutionary biology. Recently, population genomic scans have become
increasingly popular for detecting population divergence as a conse-
quence of adaptation and identifying the underlying genetic architecture
of complex divergent phenotypes (Pavlidis et al., 2008; Stinchcombe
and Hoekstra, 2008; Nielsen et al., 2009a; Nosil et al., 2009). The use
of genome-wide polymorphism data allows for the partitioning of
locus-specific effects such as recombination, mutation and selection
from demographic effects (including: bottlenecks, founder effects, popu-
lation stratification and migration etc.) (Luikart et al., 2003; Stinchcombe
and Hoekstra, 2008) and also provides for functional analyses of genetic
polymorphisms to be extrapolated to a population level (Bonin, 2008).
Unlike the more conventional linkage-based QTL analysis, population
genomic scans do not rely on structured pedigree information and
controlled breeding experiments, often impractical when working with
natural populations or organisms with long generation times (Storz,
2005; Stinchcombe and Hoekstra, 2008). Furthermore, there is no
dependence on a priori phenotypic information as is the case for
association- and conventional linkage-based studies. This is particularly
advantageous when phenotypic traits are not readily observable or
unknown, such as biochemical or physiological traits (Storz, 2005;
Walsh, 2008).
Recently, F
st
-outlier tests became popular, because it allowed for
the simultaneous analysis of a large number of loci and both domi-
nant and co-dominant marker data could be employed. F
st
-outlier
tests have been used in a number of studies in order to detect loci
that might be under selection (e.g. Bonin et al., 2006; Paris et al.,
2010; Nunes et al., 2011) including those for aquatic species, such
as, Atlantic salmon (Salmo salar; Vasemägi et al., 2005), lake whitefish
(Coregonus clupeaformis; Campbell and Bernatchez, 2004), cod (Gadus
morhua; Nielsen et al., 2009b), Eastern oyster (Crassostrea virginica;
Murray and Hare, 2006) and periwinkle snail (Littorina saxatilis;
Wilding et al., 2001) (for a review: Nielsen et al., 2009a).
The South African abalone, locally known as “perlemoen” (Haliotis
midae Linnaeus, Haliotidae; Gastropoda), is an economically impor-
tant marine mollusc. The species has a wide distribution along the
cool to warm temperate regions of the South African coast. Although
historically an important fisheries species, the commercial sector
currently relies mainly on aquaculture due to the suspension of
Marine Genomics 10 (2013) 27–36
⁎ Corresponding author. Tel.: +27 21 808 5837; fax: +27 21 808 5833.
E-mail address: clintr@sun.ac.za (C. Rhode).
1874-7787/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.margen.2013.03.001
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