Esther D. Ellen

Multilevel selection 2: Estimating the genetic parameters determining inheritance and response to selection.

Interactions among individuals are universal, both in animals and in plants and in natural as well as domestic populations. Understanding the consequences of these interactions for the evolution of populations by either natural or artificial selection requires knowledge of the heritable components underlying them. Here we present statistical methodology to estimate the genetic parameters determining response to multilevel selection of traits affected by interactions among individuals in general populations. We apply these methods to obtain estimates of genetic parameters for survival days in a population of layer chickens with high mortality due to pecking behavior. We find that heritable variation is threefold greater than that obtained from classical analyses, meaning that two-thirds of the full heritable variation is hidden to classical analysis due to social interactions. As a consequence, predicted responses to multilevel selection applied to this population are threefold greater than classical predictions. This work, combined with the quantitative genetic theory for response to multilevel selection presented in an accompanying article in this issue, enables the design of selection programs to effectively reduce competitive interactions in livestock and plants and the prediction of the effects of social interactions on evolution in natural populations undergoing multilevel selection.

Survival of Laying Hens: Genetic Parameters for Direct and Associative Effects in Three Purebred Layer Lines

Mortality due to cannibalism is a major problem in laying hens. Due to prohibition of beak-trimming in the European Union, this problem will increase in the near future. One solution to reduce mortality due to cannibalism is to use genetic selection. Mortality due to cannibalism, however, differs from conventional breeding traits, because it depends on social interactions among individuals. Selection strategies aiming to reduce cannibalism, therefore, should consider both the direct effect of an individual on its own survival and the social effect of the individual on the survival of its group members (the so-called associative effect). Traditional breeding, however, accounts for only the direct effect. Recently, methods have been proposed to estimate variance components and breeding values for both direct and associative effects. This paper presents estimated genetic parameters for direct and associative effects on survival days in 3 purebred laying lines. For the analysis, 16,780 hens with intact beaks were used. When considering only direct effects, heritabilities ranged from 2 through 10%. When considering both direct and associative effects, the total heritable variance, expressed as a proportion of phenotypic variance, ranged from 6 through 19%. These results show that heritable variation in survival days is substantially larger than suggested by conventional direct effects models. This means that prospects for reducing mortality by means of genetic selection are good and may lead to substantial reduction of 1 of the major welfare problems in egg production.

Genetic Improvement of Traits Affected by Interactions Among Individuals: Sib Selection Schemes

Livestock populations are usually kept in groups. As a consequence, social interactions among individuals affect productivity, health, and welfare. Current selection methods (individual selection), however, ignore those interactions and yield suboptimal or in some cases even negative responses. In principle, selection between groups instead of individuals offers a solution, but has rarely been adopted in practice for two reasons. First, the relationship between group selection theory and common animal breeding concepts, such as the accuracy of selection, is unclear. Second, application of group selection requires keeping selection candidates in groups, which is often undesirable in practice. This work has two objectives. First, we derive expressions for the accuracy of individual and group selection, which provides a measurement of quality for those methods. Second, we investigate the opportunity to improve traits affected by interactions by using information on relatives kept in family groups, while keeping selection candidates individually. The accuracy of selection based on relatives is shown to be an analogy of the classical expression for traits not affected by interactions. Our results show that selection based on relatives offers good opportunities for effective genetic improvement of traits affected by interactions.

Group selection and social evolution in domesticated animals.

Social interactions, especially those involving competition among individuals, are important in domesticated livestock and in natural populations. The heritability of traits affected by such interactions has two components, one originating in the individual like that of classical traits (direct effects) and the other originating in other group members (indirect effects). The latter type of trait represents a significant source of ‘hidden heritability’ and it requires population structure and knowledge from relatives in order to access it for selective breeding. When ignored, competitive interactions may increase as an indirect response to direct selection, resulting in diminished yields. We illustrate how population genetic structure affects the response to selection of traits with indirect genetic effects using population genetic and quantitative genetic theory. Population genetic theory permits us to connect our results to the existing body of theory on kin and group selection in natural populations. The quantitative genetic perspective allows us to see how breeders have used knowledge from relatives and family selection in the domestication of plants and animals to improve the welfare and production of livestock by incorporating social genetic effects in the breeding program. We illustrate the central features of these models by reviewing empirical studies from domesticated chickens.

Maternal care and selection for low mortality affect post-stress corticosterone and peripheral serotonin in laying hens.

The aim of the present study was to investigate the effect of brooding and group selection for low mortality on post-stress corticosterone and peripheral serotonin in laying hens. Birds in the experiment originated from the same population and were either group-selected for low mortality (low mortality line) or randomly selected (control line) for two generations. Twelve groups of seven birds from each line were used. Within each line, six groups were brooded by a foster mother and six groups were non-brooded. At 33 weeks of age, birds (n=42/treatment) were manually restrained for 5 min, during which their behavioral response (number of struggles) was studied. Fifteen minutes after the start of the manual restraint, blood samples were drawn for assessment of plasma corticosterone and whole blood serotonin (5-HT) concentration. In the low mortality line, 80% of the birds struggled and vocalized vs. 72% in the control line (non significant). Birds from the control line had a higher plasma corticosterone concentration after manual restraint than birds from the low mortality line (7.7 vs. 6.0 nmol ml(-1)). Furthermore, birds from the control line that were reared without a mother had a lower whole-blood 5-HT concentration than birds from the other treatments (45 vs. 48 nmol ml(-1)). These results indicate that both brooding and selection for low mortality affect post-stress corticosterone and peripheral serotonin concentration, which may result in a reduced propensity to develop feather pecking.

Indirect Genetic Effects for Survival in Domestic Chickens (Gallus gallus) Are Magnified in Crossbred Genotypes and Show a Parent-of-Origin Effect

Through social interactions, individuals can affect one another’s phenotype. The heritable effect of an individual on the phenotype of a conspecific is known as an indirect genetic effect (IGE). Although IGEs can have a substantial impact on heritable variation and response to selection, little is known about the genetic architecture of traits affected by IGEs. We studied IGEs for survival in domestic chickens (Gallus gallus), using data on two purebred lines and their reciprocal cross. Birds were kept in groups of four. Feather pecking and cannibalism caused mortality, as beaks were kept intact. Survival time was shorter in crossbreds than in purebreds, indicating outbreeding depression and the presence of nonadditive genetic effects. IGEs contributed the majority of heritable variation in crossbreds (87 and 72%) and around half of heritable variation in purebreds (65 and 44%). There was no evidence of dominance variance, neither direct nor indirect. Absence of dominance variance in combination with considerable outbreeding depression suggests that survival is affected by many loci. Direct–indirect genetic correlations were moderately to highly negative in crossbreds (−0.37 ± 0.17 and −0.83 ± 0.10), but low and not significantly different from zero in purebreds (0.20 ± 0.21 and −0.28 ± 0.18). Consequently, unlike purebreds, crossbreds would fail to respond positively to mass selection. The direct genetic correlation between both crosses was high (0.95 ± 0.23), whereas the indirect genetic correlation was moderate (0.41 ± 0.26). Thus, for IGEs, it mattered which parental line provided the sire and which provided the dam. This indirect parent-of-origin effect appeared to be paternally transmitted and is probably Z chromosome linked.

The prospects of selection for social genetic effects to improve welfare and productivity in livestock

Social interactions between individuals living in a group can have both positive and negative effects on welfare, productivity, and health of these individuals. Negative effects of social interactions in livestock are easier to observe than positive effects. For example, laying hens may develop feather pecking, which can cause mortality due to cannibalism, and pigs may develop tail biting or excessive aggression. Several studies have shown that social interactions affect the genetic variation in a trait. Genetic improvement of socially-affected traits, however, has proven to be difficult until relatively recently. The use of classical selection methods, like individual selection, may result in selection responses opposite to expected, because these methods neglect the effect of an individual on its group mates (social genetic effects). It has become clear that improvement of socially-affected traits requires selection methods that take into account not only the direct effect of an individual on its own phenotype but also the social genetic effects, also known as indirect genetic effects, of an individual on the phenotypes of its group mates. Here, we review the theoretical and empirical work on social genetic effects, with a focus on livestock. First, we present the theory of social genetic effects. Subsequently, we evaluate the evidence for social genetic effects in livestock and other species, by reviewing estimates of genetic parameters for direct and social genetic effects. Then we describe the results of different selection experiments. Finally, we discuss issues concerning the implementation of social genetic effects in livestock breeding programs. This review demonstrates that selection for socially-affected traits, using methods that target both the direct and social genetic effects, is a promising, but sometimes difficult to use in practice, tool to simultaneously improve production and welfare in livestock.

The relation between fearfulness in young and stress-response in adult laying hens, on individual and group level

Fearfulness of an individual can affect its sensitivity to stress, while at the same time the social situation in which an animal lives can affect its fear level. It is however unknown what the long-term effects of high fearfulness on sensitivity to stress are, on individual or group level in laying hens. We hypothesize that increased fearfulness at a young age results in increased sensitivity to stress at an adult age, and that this relation can differ between groups, due to differences in group composition. Therefore, we studied the relation between fearfulness in an Open Field (OF) test at six weeks of age and plasma-corticosterone (CORT) levels after a 5-min Manual Restraint test (MR) at 33 weeks of age, and assessed behavior in the home pen. We used birds from a low mortality line, selected for four generations on low mortality due to feather pecking and cannibalism and a control line (n=153 in total, eight pens/line). These lines are known to differ in fearfulness and stress physiology. Chicks from the low mortality line were more active in the OF compared to chicks from the control line. Chicks that showed a fearful response (no walking, no vocalizing) in the OF test had higher CORT at 33 weeks of age than chicks that walked and/or vocalized in the OF test and had higher activity in the home pen as adults. On group level, a passive response in the OF was related to high CORT levels after MR. Presence of at least one fearful bird in a group led to higher CORT in the other group mates compared to birds from groups with no fearful birds present. Birds from groups in which more than 50% of birds had severe comb lesions had higher CORT levels compared to birds from groups with less than 50% of birds affected. High fearfulness of laying hen chicks can on individual level have a long-term effect on stress sensitivity. The presence of fearful birds in a group as well as signs of social instability in a group, indicated by comb lesions, can affect sensitivity to stress of birds from the same group. The mechanism by which this occurs can lie in social transmission of (fear related) behavior, but this suggestion needs further investigation.

Effects of feather pecking phenotype (severe feather peckers, victims and non-peckers) on serotonergic and dopaminergic activity in four brain areas of laying hens (Gallus gallus domesticus)

Severe feather pecking (SFP) in laying hens is a detrimental behavior causing loss of feathers, skin damage and cannibalism. Previously, we have associated changes in frontal brain serotonin (5-HT) turnover and dopamine (DA) turnover with alterations in feather pecking behavior in young pullets (28-60 days). Here, brain monoamine levels were measured in adult laying hens; focusing on four brain areas that are involved in emotional behavior or are part of the basal ganglia-thalamopallial circuit, which is involved in obsessive compulsive disorders. Three behavioral phenotypes were studied: Severe Feather Peckers (SFPs), Victims of SFP, and Non-Peckers (NPs). Hens (33 weeks old) were sacrificed after a 5-min manual restraint test. SFPs had higher 5-HIAA levels and a higher serotonin turnover (5-HIAA/5-HT) in the dorsal thalamus than NPs, with intermediate levels in victims. NPs had higher 5-HT levels in the medial striatum than victims, with levels of SFPs in between. 5-HT turnover levels did not differ between phenotypes in medial striatum, arcopallium and hippocampus. DA turnover levels were not affected by feather pecking phenotype. These findings indicate that serotonergic neurotransmission in the dorsal thalamus and striatum of adult laying hens depends on differences in behavioral feather pecking phenotype, with, compared to non-pecking hens, changes in both SFP and their victims. Further identification of different SFP phenotypes is needed to elucidate the role of brain monoamines in SFP.

Estimation of heritability and breeding values for early egg production in laying hens from pooled data

Under commercial conditions, data on egg production in laying hens are usually collected per cage rather than individually. In current breeding programs, genetic evaluations are, however, based on individually recorded egg production. Because commercial flocks are not maintained in single cages, this environmental difference between the breeding and commercial setting may result in a genotype x environment interaction. This study was aimed at estimating genetic parameters and predicting estimated breeding values for early egg production of laying hens by using pooled data (i.e., data from multiple bird cages) from pedigree birds housed in 4-bird cages. Using cage records, we compared 2 different methods of handling pooled data: cage sums and the assignment of cage means to individual birds, referred to as the approximate method. The 2 methods were compared by using cross-validation. Data from 3 purebred White Leghorn layer lines were used. Estimated heritability for early egg production was 0.36 when cage sums were used and 0.30 with the approximate method. The correlation of estimated breeding values between the cage sums method and the approximate method was 0.88. Cross-validation showed that the use of cage sums led to better predictions of missing phenotypes compared with the approximate method. The results of the research demonstrate that pooled data can be used in the genetic evaluation of laying hens and show that using directly pooled records (e.g., cage sums) gives better results than assigning group means to the birds of the group, thus simulating individual records.