Indirect genetic effects from ecological interactions in Arabidopsis thaliana

Abstract

Indirect genetic effects arise when genes expressed in one individual affect the expression of traits in other individuals. The importance of indirect genetic effects has been recognized for a diversity of evolutionary processes including kin selection, sexual selection, community structure and multilevel selection, but data regarding their genetic architecture and prevalence throughout the genome remain scarce, especially for interactions between unrelated individuals. Using a set of 411 Bay-0 x Shahdara Arabidopsis recombinant inbred lines grown with Landsberg neighbours, we examined quantitative trait loci (QTL) having direct and indirect effects on size, developmental, and fitness related traits. Using an interval mapping approach, we identified 15 QTL with direct effects and found that 13 of these QTL had significant indirect effects on trait expression in neighbouring plants. These results suggest widespread pleiotropy, as nearly all direct effect QTL have associated pleiotropic indirect effects. Paradoxically, most indirect effects were of the same sign as direct effects, creating a pattern of nearly universal positive pleiotropy that makes most covariances between direct and indirect effects positive. These results are consistent with a complex genetic basis for intraspecific interactions, but suggest that interactions between neighbouring plants are largely positive, rather than negative as would be expected for competition. In addition to their evolutionary and ecological importance, these pleiotropic relationships between DGE and IGE loci have implications for quantitative genetic studies of natural populations as well as experimental design considerations. Additionally, studies that ignore IGEs may over- or underestimate quantitative genetic parameters, as well as the effect of and variance contributed by QTL.

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

“…Hence, prospects for genetic improvement of wood production appear to be considerably smaller than judged from ordinary heritabilities of bark diameter. In A. thaliana, in contrast, Mutic and Wolf (2007) found positive pleiotropic direct and indirect effects on size-, development-and fitness-related traits. Results of Peeters et al (2012) in laying hens suggest that non-additive effects may have substantial impact on the direct-indirect genetic correlation.…”

“…Evidence is increasing that IGEs can make a meaningful contribution to heritable variation in populations (for example, Mutic and Wolf, 2007;Peeters et al, 2012). IGEs can, therefore, contribute to response to selection, at least in the short term.…”

“…In total, Biscarini et al (2010) detected 11 significant direct associations between single nucleotide polymorphisms (SNPs) and feather damage, and 81 significant indirect associations. Mutic and Wolf (2007) investigated the genetic architecture of size-, development-and fitness-related traits in Arabidopsis thaliana, and identified 15 quantitative trait loci (QTL) with direct effects. Of those 15 QTL, 13 also had significant indirect effects on trait expression in neighbouring plants, suggesting wide-spread pleiotropy.…”

“…The classical example of an IGE is the maternal genetic effect of a mother on the trait values of her offspring in a mammal (Dickerson, 1947;Willham, 1963;Falconer, 1965;Kirkpatrick and Lande, 1989). Other examples of IGEs are mortality due to cannibalistic interactions in domestic chicken (Muir, 1996(Muir, , 2005, the effect of competition among trees on growth rate in bark diameter (Brotherstone et al, 2011), the outcome of dyadic interactions in deer , social behaviours in microorganisms (Crespi, 2001), size, developmental and fitness-related traits in Arabidopsis (Mutic and Wolf, 2007;Wolf et al, 2011), and growth rate in Medaka (Ruzzante and Doyle, 1991).…”

Growing with siblings: a common ground for cooperation or for fiercer competition among plants?

“…However, mechanisms that induce change in the developmental program of a plant in response to a neighbour's performance are described in the literature, providing ground for a direct link between kin recognition and kin selection. For instance, expression of certain fitness-related genes in Arabidopsis thaliana has indirect, pleiotropic effects on trait expression in neighbouring plants, but how pleiotropic effects are modulated by genetic relatedness among neighbours is unknown (Mutic & Wolf 2007).…”