Indirect Genetic Effects and Housing Conditions in Relation to Aggressive Behaviour in Pigs

Abstract

Indirect Genetic Effects (IGEs), also known as associative effects, are the heritable effects that an individual has on the phenotype of its social partners. Selection for IGEs has been proposed as a method to reduce harmful behaviours, in particular aggression, in livestock and aquaculture. The mechanisms behind IGEs, however, have rarely been studied. The objective was therefore to assess aggression in pigs which were divergently selected for IGEs on growth (IGEg). In a one generation selection experiment, we studied 480 offspring of pigs (Sus scrofa) that were selected for relatively high or low IGEg and housed in homogeneous IGEg groups in either barren or enriched environments. Skin lesion scores, a proxy measure of aggression, and aggressive behaviours were recorded. The two distinct IGEg groups did not differ in number of skin lesions, or in amount of reciprocal fighting, both under stable social conditions and in confrontation with unfamiliar pigs in a 24 h regrouping test. Pigs selected for a positive effect on the growth of their group members, however, performed less non-reciprocal biting and showed considerably less aggression at reunion with familiar group members after they had been separated during a 24 h regrouping test. The enriched environment was associated with more skin lesions but less non-reciprocal biting under stable social conditions. Changes in aggression between pigs selected for IGEg were not influenced by G×E interactions with regard to the level of environmental enrichment. It is likely that selection on IGEg targets a behavioural strategy, rather than a single behavioural trait such as aggressiveness.

Indirect genetic effects in behavioral ecology: does behavior play a special role in evolution?

“…The strength and direction of IGEs can also evolve over time and across populations (Chenoweth et al 2010;Bailey and Zuk 2012;Kazancioğlu et al 2012;Edenbrow et al 2017), and associated social selection is predicted to vary accordingly (McGlothlin et al 2010). In recent years, IGEs have been incorporated into animal and plant breeding studies to more accurately predict evolutionary responses in agriculturally valuable traits, such as growth rate, thermal tolerance, and infection risk (Camerlink et al 2013(Camerlink et al , 2014(Camerlink et al , 2015Costa e Silva et al 2013;Anche et al 2014;Muñoz et al 2014;Alemu et al 2016;Baud et al 2017). A substantial literature explores the mathematical approaches used to study IGEs.…”

“…Examples of both are readily found in the literature. For example, IGEs on growth in pigs arising from behavioral phenotypes such as aggressive biting are not only documented, but have been successfully selected in artificial breeding programs (Camerlink et al 2013(Camerlink et al , 2014. In contrast, isogenic focal Drosophila melanogaster males vary in how much they physically tap interacting partners of different genotypes with their prothoracic legs during bouts of interaction lasting only minutes, a behavior that might reflect gustatory sampling or aggression (Bailey and Hoskins 2014).…”

“…Thus, this behavior would appear counterintuitive, or nonoptimal, if IGEs are not considered. Other examples exist in the field of animal breeding, in which programs considering IGEs have been shown to improve the response of selection for various traits of interest to breeders (e.g., growth rates in pigs, or plumage condition in laying hens) (Camerlink et al 2013(Camerlink et al , 2015Brinker et al, 2014). In Table 1, we provide additional examples illustrating how considering IGEs can modify our interpretations of a behavior's causes, and reveal unsuspected evolutionary forces influencing their expression.…”

Social structure and indirect genetic effects: genetics of social behaviour

“…Ecological interactions in plant systems contribute to the size and fitness-related traits of neighbours (Mutic & Wolf, 2007;Wolf, Mutic & Kover, 2011;Andersson, 2014), which has led to accounting for IGEs in the optimization of breeding programs (Muir, 2005). Examples of phenotypes under shared genetic control from the animal kingdom include social dominance interactions in red deer Cervus elaphus (Wilson et al, 2011), antipredator behaviour in Poecilia reticulate guppies (Bleakley & Brodie, 2009), growth rate in medaka Oryzias latipes (Ruzzante & Doyle, 1991), female choosiness in Pacific field crickets Teleogryllus oceanicus (Bailey & Zuk, 2012), egg-laying date variance in common gulls Larus canus (Brommer & Rattiste, 2008), as well as aggression in pigs Sus scrofa (Camerlink et al, 2013) and mink Neovison vison (Alemu et al, 2014). Yet another ubiquitous category is intergenerational IGEs best exemplified by maternal effects in plants (Roach & Wulff, 1987), insects (Mousseau et al, 2009), and animals (Bernardo, 1996).…”

Genetics of inherited variability : Increasing uniformity by reducing competition

“…Such interactions have been well-documented for laying hens, where cannibalistic behavior causes mortality (Muir, 1996;, and for pigs, where competition and tail biting leads to poorer growth and reduced animal welfare (Arango et al, 2005;Camerlink et al, 2013Camerlink et al, , 2014Bergsma et al, 2013). In fish species, social interactions such as aggression and competition have been studied for their detrimental effect on growth of the population (medaka, Ruzzante and Doyle, 1991;Atlantic cod, Monsen et al, 2008; Nile tilapia, .…”