Genetic control of interactions among individuals: contrasting outcomes of indirect genetic effects arising from neighbour disease infection and competition in a forest tree

Abstract

Indirect genetic effects (IGEs) are heritable effects of individuals on trait values of their conspecifics. IGEs may substantially affect response to selection, but empirical studies on IGEs are sparse and their magnitude and correlation with direct genetic effects are largely unknown in plants. Here we used linear mixed models to estimate genetic (co)variances attributable to direct and indirect effects for growth and foliar disease damage in a large pedigreed population of Eucalyptus globulus. We found significant IGEs for growth and disease damage, which increased with age for growth. The correlation between direct and indirect genetic effects was highly negative for growth, but highly positive for disease damage, consistent with neighbour competition and infection, respectively. IGEs increased heritable variation by 71% for disease damage, but reduced heritable variation by 85% for growth, leaving nonsignificant heritable variation for later age growth. Thus, IGEs are likely to prevent response to selection in growth, despite a considerable ordinary heritability. IGEs change our perspective on the genetic architecture and potential response to selection. Depending on the correlation between direct and indirect genetic effects, IGEs may enhance or diminish the response to natural or artificial selection compared with that predicted from ordinary heritability.

The quantitative genetics of indirect genetic effects: a selective review of modelling issues

“…This will cause the gradual exhaustion of heritable variation and the build-up of a trade-off between the direct and indirect components of the total breeding value. Results confirming this expectation have been found in the tree species E. globulus and Pinus taeda L., where DGE and IGE for bark diameter show a correlation of around À0.8 Brotherstone et al, 2011;Costa e Silva et al, 2013). Such negative correlations between DGEs and IGEs may severely reduce the potential for genetic improvement of bark diameter in forestry (Costa e Silva et al, 2013).…”

“…Results confirming this expectation have been found in the tree species E. globulus and Pinus taeda L., where DGE and IGE for bark diameter show a correlation of around À0.8 Brotherstone et al, 2011;Costa e Silva et al, 2013). Such negative correlations between DGEs and IGEs may severely reduce the potential for genetic improvement of bark diameter in forestry (Costa e Silva et al, 2013). Hence, prospects for genetic improvement of wood production appear to be considerably smaller than judged from ordinary heritabilities of bark diameter.…”

“…On the other hand, IGEs may fully remove heritable variation, despite a significant ordinary heritability (Bijma, 2011;Wilson et al, 2011;Costa e Silva et al, 2013). Thus, as interactions among individuals are abundant in nature (for example, Frank, 2007), the heritable variance that determines the potential of a population to respond to selection will usually differ from the ordinary additive genetic variance, but the magnitude of this difference is largely unknown at present.…”

“…In populations of plants, including trees, spatial residual variance structures may be fitted to account for local environmental trend and for the non-genetic component of the indirect effect. In tree breeding, advanced modelling strategies have been developed to account for such effects (Gilmour et al, 1997;Stringer et al, 2011;Costa e Silva et al, 2013).…”

“…In general, the strength of the interactions may vary among pairs of individuals,for example, because of variation in distance among plants or variation in group size in animals. To account for such effects in the statistical model, IGEs may be multiplied by factors (Muir, 2005;Cantet and Cappa, 2008;Cappa and Cantet, 2008;Bijma, 2010a; Costa e Silva et al, 2013),…”