---
_id: '7751'
abstract:
- lang: eng
text: "This work demonstrates that environmental conditions experienced by individuals
can shape their development and affect the stability of genetic associations.
The implication of this observation is that the environmental response may influence
the evolution of traits in the wild. Here, we examined how the genetic architecture
of a suite of sexually dimorphic traits changed as a function of environmental
conditions in an unmanaged population of Soay sheep (Ovis aries) on the island
of Hirta, St. Kilda, northwest Scotland. We examined the stability of phenotypic,
genetic, and environmental (residual) covariance in males during the first year
of life between horn length, body weight, and parasite load in environments of
different quality. We then examined the same covariance structures across environments
within and between the adult sexes. We found significant genotype-by-environment
interactions for lamb male body weight and parasite load, leading to a change
in the genetic correlation among environments. Horn length was genetically correlated
with body weight in males but not females and the genetic correlation among traits
within and between the sexes was dependent upon the environmental conditions experienced
during adulthood. Genetic correlations were smaller in more favorable environmental
conditions, suggesting that in good environments, loci are expressed that have
sex-specific effects. The reduction in genetic correlation between the sexes may
allow independent evolutionary trajectories for each sex. This study demonstrates
that the genetic architecture of traits is not stable under temporally varying
environments and highlights the fact that evolutionary processes may depend largely
upon ecological conditions.\r\nENVIRONMENTAL heterogeneity has long been recognized
as an important factor influencing the evolution of fitness-related traits in
the wild (Roff 2002). The evolution of a trait depends upon the selection upon
it, underlying genetic variation, and to a large degree the genetic relationships
with other traits (Lynch and Walsh 1998). There is evidence that selection can
vary considerably from year to year (Price et al. 1984; Robinson et al. 2008)
and genetic variability in quantitative traits can change in response to environmental
conditions (Hoffmann and Merilä 1999; Charmantier and Garant 2005). However, we
know surprisingly little about the influence of environmental conditions on genetic
correlations between traits in wild populations. Laboratory evidence suggests
that the environment may influence genetic relationships between traits (Sgrò
and Hoffmann 2004), but estimates obtained in a controlled or in an arbitrary
range of conditions show a lack of concordance with those obtained in wild habitats
(Conner et al. 2003). As a result, laboratory and environment-specific estimates
of genetic correlations can make predictions for a trait's evolution, but these
are valid only for the environment in which they were measured. Therefore, at
present, it is difficult to generalize about the evolution of a trait that is
expressed in populations that experience variable environmental conditions (Steppan
et al. 2002).\r\nThe influence of changing environmental conditions on the G matrix
(the matrix of additive genetic variance and covariances corresponding to a set
of traits) has been the focus of theoretical quantitative genetic studies (e.g.,
Jones et al. 2003). There is evidence of genotype-by-environment interaction for
many traits expressed in wild populations (Charmantier and Garant 2005) and thus
we may also expect that associations between traits may depend upon the environmental
conditions encountered by an individual. Genetic correlations among traits may
arise from pleiotropy, where a given locus affects more than one trait (Cheverud
1988; Lynch and Walsh 1998), which may limit the potential for those traits to
evolve independently. There has recently been much interest in assessing genetic
correlations between the sexes (Rice and Chippindale 2001; Foerster et al. 2007;
Poissant et al. 2008), but all of these predictions have also been made in average
environmental conditions. For sexually dimorphic traits, expectations of between-sex
genetic correlations are unclear (Lande 1980; Badyaev 2002). We might expect that
the genetic determination of a trait and the patterns of genetic covariance between
traits may differ both within and between the sexes, producing the differences
in trait growth that are commonly observed (Lande 1980; Badyaev 2002; Roff 2002),
but so far evidence suggests that genetic expression in both sexes is influenced
by the same developmental pathway (Roff 2002; Jensen et al. 2003; Parker and Garant
2005). However, to our knowledge, no study has yet determined whether genetic
correlations, both within and between the sexes, vary across gradients of the
environmental conditions encountered by individuals in the wild (Garant et al.
2008).\r\nThis study aims to assess the stability of phenotypic, genetic, and
environmental (residual) associations between traits, within and between the sexes,
across a range of environmental conditions experienced by a wild population. We
focus on the traits of horn length, body weight, and parasite load in a feral
population of Soay sheep (Ovis aries) from the island of Hirta, St. Kilda, United
Kingdom. Weather conditions, population density, and consequently resource availability
fluctuate from year to year, providing substantial differences between individuals
in the environments they experience and thus their survival rates (Clutton-Brock
and Pemberton 2004). These varying conditions, combined with a large pedigree
and extensive repeated morphological measures, provide an excellent opportunity
to assess the potential effects of environmental heterogeneity on genetic architecture
of traits. Previous studies on this population have shown additive genetic variance
for many morphological traits (Milner et al. 2000; Coltman et al. 2001; Wilson
et al. 2005), genetic correlations between traits (Coltman et al. 2001), and genotype-by-environment
interactions for birth weight (Wilson et al. 2006). Here we apply a random regression
animal model approach to assess the extent to which quantitative genetic parameters
of a range of morphological traits measured during life vary as a function of
environmental conditions. We then extend this methodology to the multivariate
case, testing whether the phenotypic covariance structure, and the underlying
G matrix, depends on the environmental conditions experienced. Since the traits
considered here are known to be sexually dimorphic and there are differences in
trait growth and survival across ages, we look at sex-specific traits in lambs
and then across all ages."
article_processing_charge: No
article_type: original
author:
- first_name: Matthew Richard
full_name: Robinson, Matthew Richard
id: E5D42276-F5DA-11E9-8E24-6303E6697425
last_name: Robinson
orcid: 0000-0001-8982-8813
- first_name: Alastair J.
full_name: Wilson, Alastair J.
last_name: Wilson
- first_name: Jill G.
full_name: Pilkington, Jill G.
last_name: Pilkington
- first_name: Tim H.
full_name: Clutton-Brock, Tim H.
last_name: Clutton-Brock
- first_name: Josephine M.
full_name: Pemberton, Josephine M.
last_name: Pemberton
- first_name: Loeske E. B.
full_name: Kruuk, Loeske E. B.
last_name: Kruuk
citation:
ama: Robinson MR, Wilson AJ, Pilkington JG, Clutton-Brock TH, Pemberton JM, Kruuk
LEB. The impact of environmental heterogeneity on genetic architecture in a wild
population of soay sheep. Genetics. 2009;181(4):1639-1648. doi:10.1534/genetics.108.086801
apa: Robinson, M. R., Wilson, A. J., Pilkington, J. G., Clutton-Brock, T. H., Pemberton,
J. M., & Kruuk, L. E. B. (2009). The impact of environmental heterogeneity
on genetic architecture in a wild population of soay sheep. Genetics. Genetics
Society of America. https://doi.org/10.1534/genetics.108.086801
chicago: Robinson, Matthew Richard, Alastair J. Wilson, Jill G. Pilkington, Tim
H. Clutton-Brock, Josephine M. Pemberton, and Loeske E. B. Kruuk. “The Impact
of Environmental Heterogeneity on Genetic Architecture in a Wild Population of
Soay Sheep.” Genetics. Genetics Society of America, 2009. https://doi.org/10.1534/genetics.108.086801.
ieee: M. R. Robinson, A. J. Wilson, J. G. Pilkington, T. H. Clutton-Brock, J. M.
Pemberton, and L. E. B. Kruuk, “The impact of environmental heterogeneity on genetic
architecture in a wild population of soay sheep,” Genetics, vol. 181, no.
4. Genetics Society of America, pp. 1639–1648, 2009.
ista: Robinson MR, Wilson AJ, Pilkington JG, Clutton-Brock TH, Pemberton JM, Kruuk
LEB. 2009. The impact of environmental heterogeneity on genetic architecture in
a wild population of soay sheep. Genetics. 181(4), 1639–1648.
mla: Robinson, Matthew Richard, et al. “The Impact of Environmental Heterogeneity
on Genetic Architecture in a Wild Population of Soay Sheep.” Genetics,
vol. 181, no. 4, Genetics Society of America, 2009, pp. 1639–48, doi:10.1534/genetics.108.086801.
short: M.R. Robinson, A.J. Wilson, J.G. Pilkington, T.H. Clutton-Brock, J.M. Pemberton,
L.E.B. Kruuk, Genetics 181 (2009) 1639–1648.
date_created: 2020-04-30T11:01:57Z
date_published: 2009-04-01T00:00:00Z
date_updated: 2021-01-12T08:15:17Z
day: '01'
doi: 10.1534/genetics.108.086801
extern: '1'
intvolume: ' 181'
issue: '4'
language:
- iso: eng
month: '04'
oa_version: None
page: 1639-1648
publication: Genetics
publication_identifier:
issn:
- 0016-6731
- 1943-2631
publication_status: published
publisher: Genetics Society of America
quality_controlled: '1'
status: public
title: The impact of environmental heterogeneity on genetic architecture in a wild
population of soay sheep
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 181
year: '2009'
...