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Impact of Nonrandom Mating on Genetic Variance and Gene Flow in Populations with Mass Selection
Léopoldo Sanchez, John Woolliams
To cite this version:
Léopoldo Sanchez, John Woolliams. Impact of Nonrandom Mating on Genetic Variance and Gene
Flow in Populations with Mass Selection. Genetics, Genetics Society of America, 2004, 166 (1),
pp.527-535. �hal-02677824�
Copyright 2004 by the Genetics Society of America
Impact of Nonrandom Mating on Genetic Variance and Gene Flow in Populations With Mass Selection
Leopoldo Sa´nchez 1 and John A. Woolliams
Roslin Institute (Edinburgh), Roslin, Midlothian EH25 9PS, United Kingdom Manuscript received March 19, 2002
Accepted for publication September 19, 2003
ABSTRACT
The mechanisms by which nonrandom mating affects selected populations are not completely under- stood and remain a subject of scientific debate in the development of tractable predictors of population characteristics. The main objective of this study was to provide a predictive model for the genetic variance and covariance among mates for traits subjected to directional selection in populations with nonrandom mating based on the pedigree. Stochastic simulations were used to check the validity of this model. Our predictions indicate that the positive covariance among mates that is expected to result with preferential mating of relatives can be severely overpredicted from neutral expectations. The covariance expected from neutral theory is offset by an opposing covariance between the genetic mean of an individual’s family and the Mendelian sampling term of its mate. This mechanism was able to predict the reduction in covariance among mates that we observed in the simulated populations and, in consequence, the equilib- rium genetic variance and expected long-term genetic contributions. Additionally, this study provided confirmatory evidence on the postulated relationships of long-term genetic contributions with both the rate of genetic gain and the rate of inbreeding (⌬F ) with nonrandom mating. The coefficient of variation of the expected gene flow among individuals and ⌬F was sensitive to nonrandom mating when heritability was low, but less so as heritability increased, and the theory developed in the study was sufficient to explain this phenomenon.
R ECENT advances in quantitative genetic theory female, has been less well studied in this context. Al- though utilizing a mating design to minimize ⌬F does have allowed breeding schemes to consider the
not always lead to substantial deviations from HW pro- management of genetic variation objectively, simultane-
portions (Sonesson and Meuwissen 2000), much of ously with the maximization of genetic gain. Such ad-
the theory on genetic variation and the impact of non- vances are highly relevant to breeding practice, not only
random mating has been built up around the concept for commercial schemes but also for those schemes that
of departures from HW equilibrium (e.g., Caballero are orientated toward the conservation of genetic re-
and Hill 1992; Santiago and Caballero 1995; Wang sources. These advances include the development of
1996) and the concepts of the avoidance of, or prefer- tractable, deterministic predictors of rates of inbreeding
ence for, mating relatives.
(⌬F ), gene flow, and genetic gain (⌬G ) for complex
The interpretation of the work on nonrandom mat- selected populations (Woolliams et al. 1999; Woolli-
ing, both its application and its impact, remains a subject ams and Bijma 2000), and operational tools for day-
of scientific debate. For example, in conservation, ac- to-day selection decisions (Wray and Goddard 1994;
cepted practice uses minimum coancestry to minimize Meuwissen 1997; Grundy et al. 1998).
⌬F (Caballero et al. 1996; Frankham et al. 2002), yet However, the theory underpinning these tools has
recent theoretical developments using genetic contribu- been developed primarily for random mating of the
tions show that the lowest ⌬F with hierarchical matings selected males and females and for a neutral locus where
is achievable when relatives are preferentially mated the genotypic frequencies in the offspring display no
(Sa´nchez et al. 2003). In selected populations, there is departure from Hardy-Weinberg (HW) proportions,
clear evidence that mating designs are beneficial, al- other than that arising from the partitioning of the gene
though not all these designs define matings through pool induced by two sexes (Robertson 1965). However,
pedigree, e.g., factorial mating (Woolliams 1989).
the role of nonrandom mating, where some specific
Several articles indicate that attention to the pedigree design is placed upon which male is mated to which
relationships within a mating design can be advanta- geous over random-mating schemes (e.g., Santiago and Caballero 1995; Caballero et al. 1996; Sa´nchez et al.
1
Corresponding author: INRA-Orle´ans, Unite´ d’Ame´lioration, Ge´n- 1999). However, the benefits of these methods have not
e´tique et Physiologie des Arbres Forestiers, Ave. de la Pomme de Pin,
always been quantified in predictable terms for their
Ardon, B.P. 20619-45166 Olivet Cedex, France.
E-mail: leopoldo.sanchez@orleans.inra.fr joint impact upon genetic gain and rates of inbreeding.
Genetics 166: 527–535 ( January 2004)
viduals), it measures the actual loss of heterozygosity due to Moreover, other studies on mating designs (Toro and
the nonrandomness of the mating of the parents with nonzero Pe´rez-Enciso 1990; Klieve et al. 1994; Ferna´ndez and
contributions in the offspring generation (often denoted as Toro 1999) do not separate out the impact of specifying ␣
I
). Thus the former (␣
O) is a potential correlation of uniting the matings from the impact of controlling only the gametes from selected parents, whereas the latter (␣
I) is a realized correlation and will be affected by the finite random overall contribution of each selected individual assum-
sampling of gametes to form the offspring generation and ing random mating.
by any artificial and/or natural selection of offspring before Santiago and Caballero (1995) were successful in
reaching the breeding population.
producing predictions of the effective population size Under the assumption of completely neutral genes ␣
Owould [N
e, defined as (2⌬F ) ⫺
1] in nonrandom mating popula- tend to be equal to ␣
I. For neutral genes, when nonrandom mating results from a mix of full-sib mating and random mat- tions undergoing mass selection, using an approach
ing, ␣
I(i.e., ␣
I⬇␣
O⫽ ␣) can be related to the proportion of based upon the variance of allele frequencies. These
full-sib mating (denoted hereafter φ) by ␣ ⫽ φ/(4 ⫺ 3φ) (Ghai authors considered nonrandom mating in the form of
1969).
departures from HW equilibrium achieved through par- To obtain ␣
O
in a breeding population, let
ijbe the coances- tial full-sib mating. However, Woolliams and Bijma try (kinship) coefficient (Lynch and Walsh 1998) of sire i and dam j, then following Wright’s (1969) equation 1 ⫺ ␣
O(i,j)⫽ (2000) showed that, for random mating, an approach
(1 ⫺
ij)/(1 ⫺ ), where ⫽ F
STis the average of all the entries to predicting N
eusing long-term genetic contributions
in the matrix of coancestries among the parents (i.e., i, j, and was capable of extension to more complex selection
contemporaries), including self-coancestries and the recipro- schemes. To achieve such an extension with nonrandom cals (Cockerham 1967). Thus ␣
O(i,j)is defined for any pair of mating requires an understanding of the expected gene parents in relation to the complete set of selected parents.
The term ␣
Ois the average ␣
O(i,j)of the selected matings, flows of individuals based upon the inheritance of selec-
irrespective of the fitness of the offspring, i.e., as if all matings tive advantages, which in turn presupposes an understand-
contribute an equal and large number of offspring to the next ing of the behavior of the genetic variation. There appears
generation.
to be little published information on these topics. To obtain a summary value of ␣
Ifor a pedigreed population Therefore, the main objective of this study is to ad- undergoing selection, we follow the same reasoning as above.
Note that ⫽ F
STrepresents the average inbreeding coeffi- vance the theoretical framework for predicting the im-
cient if the offspring generation had been obtained by com- pact of nonrandom mating for populations undergoing
plete aggregation of the parental gene pool and sampling at directional selection, providing a predictive model for
random with replacement. Then for any individual offspring the genetic variance and covariance among mates. The from that set of parents ␣
I(k) ⬇F
ISand can be defined as nonrandom mating is defined solely in terms of depar- 1 ⫺ ␣
I(k)⫽ (1 ⫺ F(k))/(1 ⫺ ), where F(k) is the coefficient of inbreeding of individual k, and is equal to
sire(k),dam(k). For tures from HW proportions for neutral alleles, without
the infinitesimal model, the Mendelian sampling deviation reference to phenotypes. The impact is measured in
for an offspring k has a variance equal to terms of genetic parameters, such as genetic variance,
expected gene flow, and ⌬F, assuming the infinitesimal
122A,0
冢
1⫺12F(sire(k))⫺12F(dam(k))
冣
⫽122A,0冤
12(1⫺F(sire(k)))⫹12(1⫺F(dam(k)))
冥
model and mass selection. In the course of this article,
the opportunity to validate the developments of Wool-
⫽122A,0(1⫺ )
冢
1⫺12␣I(sire(k))⫺12␣I(dam(k))
冣
,(1)
liams and Bijma (2000) for nonrandom mating is
where
2A,0is the initial variance of the breeding values. In the taken. The accuracies of the predictions of ⌬F and ⌬G
remainder of this study, the term (1 ⫺ ) in Equation 1 is and the validity of the framework are established with
omitted for derivations and predictions, analogously to Wool- the help of stochastic simulations. liams et al. (1999) and Woolliams and Bijma (2000). This omission allows the genetic variance to reach an equilibrium.
Further details are given in the last section of materials and methods.
MATERIALS AND METHODS
The terms ␣
I(k)are used to define two related, but distinct, Nonrandom mating and neutral theory: The correlation summary ␣
I: (i) ␣
Ic⫽
兺kc
k␣
I(k), where c
kwas the observed between uniting gametes due to the nonrandom mating of contribution of k to the selected offspring in the next genera- parents is an additional factor affecting heterozygosity over tion, and (ii) ␣
Ir⫽
兺kr
k␣
I(k), where r
kwas the long-term genetic and above initial gene frequencies and their accumulated contribution (described in the following sections) of k. If we drift. Using the classical F-statistics of Wright (1969), the assume now that directional selection has taken place among expected fractional decrease in the heterozygosity for a given families, then the direct equivalence between ␣
Oand ␣
I(irre- population (F
IT) can be related to two further statistics using spective of whether Ic or Ir) no longer holds for selective the relationship (1 ⫺ F
IT) ⫽ (1 ⫺ F
IS)(1 ⫺ F
ST), where F
STis genes or neutral genes since selection success will depend on the fractional loss of heterozygosity due to the finiteness of the ␣
Iof the parents (Caballero et al. 1996).
the population census, and F
ISis the loss of heterozygosity due Dynamics of genetic (co)variance for a selected trait under
to the nonrandom mating of parents. The F
IScan be seen as nonrandom mating: In this section, a model is developed to
a correlation of gene effects between homologous alleles in show that the impact of nonrandom mating on covariances
pairs of mating parents, i.e., the correlation between alleles between mates for selected traits and neutral traits may be
within infinitely many conceptual offspring derived from each qualitatively different and to describe the circumstances under
of the pairs of mating parents (often denoted ␣
Oand hereafter which this can occur. In particular, it demonstrates that selec-
in this study). Whereas, if conceived of as the correlation tion induces a negative covariance between true family means
and Mendelian sampling terms, not only within individual
between alleles within successful offspring (i.e., existing indi-
529 Genetic Variance and Inbreeding
selected parents but also between a parent and its mate, from Equation 3 is that the covariance between mates for the selected trait may be dramatically reduced below what is thereby reducing genetic variance more than would be pre-
dicted by previously existing selection theory. expected when b
afbecomes more strongly negative, when (i) selection intensity is large, since → 1, and when (ii) h
20is Consider a population with equal numbers of dams and
sires, i.e., a mating ratio of 1, mated in pairs to produce a large, since
2M/
2Pis large. The term (1 ⫹ b
af)
2is relatively insensitive to ␣ for mass selection, but is sensitive to h
20. For deviation from HW equilibrium equal to ␣
Oon the basis of
pedigree information alone. For the trait under selection, assume ⫽ 0.64, ␣ ⫽ 0.06, (1 ⫹ b
af)
2takes values of 0.87, 0.73, 0.57, 0.38, and 0.18 for h
20⫽ 0.2, 0.4, 0.6, 0.8, and 0.99, respectively a heritability of h
20when in HW equilibrium in an unselected
base generation, with a phenotypic variance
2P,0⫽ 1. It is as- (from Equation 3 and genetic variances obtained from simu- lated populations); for ␣ ⫽ 0.24, the values are 0.90, 0.77, sumed that the inheritance of the trait under selection can
be described by an infinitesimal model and, for simplicity in 0.62, 0.42, and 0.18.
Since
2M* ⫽
2M(1 ⫺
2M/
2P),
2A* ⫽
2F* ⫹ 2 cov(f
i, a
i)* ⫹ the derivation of this model, that the nonrandom mating is
achieved by managing φ, the proportion of full-sib matings.
2M* ⫽
2A(1 ⫺ h
2), and for their offspring A
off⫽
1⁄
2(A
i⫹ A
j) ⫹ a
off:
Note that this mating scheme does not produce half-sibs. From Ghai (1969), the neutral expectations are ␣
I⫽ ␣
O⫽ ␣, and
2A⫽
1⁄
2(
2A* ⫹ φ(1 ⫹ b
af)
2
2F* ) ⫹
2M. (5) φ ⫽ 4␣/(1 ⫹ 3␣) for large populations.
Let P
idenote the phenotype of an individual i for the se- This will move to equilibrium over generations so that the lected trait and B
ibe the breeding value for a neutral trait, effect of selection is counterbalanced by the addition of
2Mthen the covariance between breeding values of mates is given (analogously to Bulmer 1980, p. 155).
by Caballero and Hill (1992) as cov(B
sire, B
dam) ⫽ 2␣
O
2B, Consequently, for the selected trait, the total observed addi- where
2Bis the variance of the breeding values in the unse- tive variance may decline even as ␣
Oincreases (demonstrated lected and randomly mated base population. Now consider in the results), although ␣
Ois superficially increasing one A
i, the breeding value for the selected trait. Then A
i⫽
1⁄
2(A
sire⫹ component of the variation. This is a phenomenon associated A
dam) ⫹ a
i⫽ f
i⫹ a
i, where f
iis the true family mean, and a
iwith linkage disequilibrium and arises from (i) a lower Mende- is the Mendelian sampling term. Define
2A,tas the variance lian sampling variance replenishing the genetic variation lost of the breeding values at time t with
2A,t⫽
2F,t⫹
2M, where due to selection in each generation and (ii) the induction of
2F,tis the variance of the true family means at time t, and negative covariance between the Mendelian sampling term of
2M⫽
1⁄
2(1 ⫺ ␣
I)h
20is the variance of the Mendelian sampling a parent and the true family mean of its mate.
terms [note that the term (1 ⫺ ) in Equation 1 is omitted Predictions of rate of inbreeding and genetic gain through here, and since
2P,0⫽ 1, h
20⫽
2A,0]. For simplicity, the explicit the concept of long-term genetic contributions: The genetic dependence on t in the notation is neglected. For selection contribution of an ancestor k (denoted r
k) to a descendant j
on phenotype P
i, is the proportion of genes carried by j that are expected to
derive by descent from the ancestor k. A descendant’s breeding f
i⫽
2F
2PP
i⫹ ε
i,1value can be decomposed into a sum of Mendelian sampling deviations from all ancestors, with the weighting for ancestor k’s Mendelian deviation being r
k. For a mixing population, a
i⫽
2M
2PP
i⫹ ε
i,2, (2) after a sufficiently large number of generations, k’s genetic contribution to all individuals within the population ap- where f
iand a
iare both partitioned into an expectation condi- proaches the same stable and constant value across genera- tional on P
iand a residual (ε). Since cov(f
i, a
i) ⫽ 0, cov(ε
1, ε
2) ⫽ tions. In the remainder of the text, the stable genetic contribu-
⫺
2F
2M/
2P. Following the methods of Bulmer (1980) for selec- tions from distant ancestors are referred to as “long-term tion with the infinitesimal model, let superscript * denote a genetic contributions.” The long-term genetic contributions parameter postselection on P
i, then cov(f
i, a
i)* ⫽ ⫺
2F
2M/
2Pwill reflect differences among individual ancestors arising since
2*P⫽ (1 ⫺ )
2P, where is the variance reduction coef- from their respective selective advantages together with cumu- ficient. This has a direct analogy to linkage disequilibrium, lative chance factors across generations. Therefore, long-term where selection on P
iinduces negative covariance between genetic contributions model the gene flow of individual ances- the effects of different loci, and where the induction of this tors through the population.
covariance is not dependent on mating procedures. The re- The asymptotic ⌬F for nonrandom mating can be derived gression of a
ion f
iafter selection is through its theoretical relationship with the sum of squared
long-term genetic contributions, b
af⬇⫺
2F
2M/(
2P
2F* ) , (3)
⌬F ⫽
1⁄
4(1 ⫺ ␣
I)
兺k
r
2k(6)
where
2F* ⫽
2F(1 ⫺
2F/
2P) is the variance of true full-sib family means after selection. Note b
af⬍ 0, and b
af⬆ 0 after selection.
(Woolliams and Bijma 2000). The rate of genetic gain (⌬G ) When allocating mates (i, j) using the pedigree alone,
per generation is also related to long-term genetic contribu- cov(A
i, A
j) ⫽ cov(f
i⫹ a
i, f
j⫹ a
j) tions since sustained genetic gain arises through the genera- tion of covariance between long-term genetic contributions
⫽ cov(f
i, f
j) ⫹ cov(f
i, a
j) ⫹ cov(f
j, a
i) ⫹ cov(a
i, a
j).
and Mendelian sampling deviations, Substituting a
j⫽ b
aff
j⫹ ε
jand analogously for a
i, and using φ
⌬G ⫽
兺k