Indirect genetic effects clarify how traits can evolve even when fitness does not

Abstract

There are many situations in nature where we expect traits to evolve but not necessarily for mean fitness to increase. However, these scenarios are hard to reconcile simultaneously with Fisher's fundamental theorem of natural selection (FTNS) and the Price identity (PI). The consideration of indirect genetic effects (IGEs) on fitness reconciles these fundamental theorems with the observation that traits sometimes evolve without any adaptation by explicitly considering the correlated evolution of the social environment, which is a form of transmission bias. Although environmental change is often assumed to be absent when using the PI, here we show that explicitly considering IGEs as change in the social environment with implications for fitness has several benefits: (1) it makes clear how traits can evolve while mean fitness remains stationary, (2) it reconciles the FTNS with the evolution of maladaptation, (3) it explicitly includes density‐dependent fitness through negative social effects that depend on the number of interacting conspecifics, and (4) it allows mean fitness to evolve even when direct genetic variance in fitness is zero, if related individuals interact and/or if there is multilevel selection. In summary, considering fitness in the context of IGEs aligns important theorems of natural selection with many situations observed in nature and provides a useful lens through which we might better understand evolution and adaptation.

The ecological causes and consequences of hard and soft selection

“…predisposition to be aggressive) alter another conspecific's fitness (i.e. indirect genetic effects; Fisher & McAdam, 2019). A range of models touch on the various genetic and evolutionary possibilities outlined above, but often without explicit mention of soft selection (Anderson & Arnold, 1983; Bürger & Gimelfarb, 2004; Clarke, 1973; Engen et al, 2020; Maynard Smith, 1968; Smouse, 1976; Sved, 1968; Svensson & Connallon, 2019).…”

“…Soft selection involving a zero‐sum game allows for rapid trait evolution over multiple generations with minimal influence on population dynamics (e.g. Fisher & McAdam, 2019), and thus high rates of sustainable evolution (e.g. Maynard Smith, 1968; Sved, 1968).…”

Inheritance of Rootstock Effects in Avocado (Persea americana Mill.) cv. Hass

“…To expand our knowledge on the extent of the rootstock–scion interaction and speed up fruit tree breeding programs ( Kumar et al, 2020 ; Peng et al, 2020 ; Santantonio and Robbins, 2020 ), further heritability estimates should be gathered on contrasting traits using multi-environment ( Crossa et al, 2019 ; Costa-Neto et al, 2020 ) provenance (“common garden”) and progeny trials with diverse panels of seedling and clonal rootstocks. The “genetic prediction” model used here to estimate pedigree-free heritabilities ( Milner et al, 2000 ; Kruuk, 2004 ; Frentiu et al, 2008 ; Wilson et al, 2010 ; Berenos et al, 2014 ), or alternatively indirect genetic effect (IGE) models ( Bijma, 2010 , 2013 ; Fisher and Mcadam, 2019 ), may be extended to field trials at a low genotyping cost, as few polymorphic SSR markers are enough to span the genetic relatedness gradient. This model suggested evidence that rootstock’s influences transcend the root phenotype and can directly impact the phenotype of the grafted scion for economically important traits.…”

“…How different genomes interact to shape a unique phenotype has been one of the most pervasive questions in quantitative genetics and molecular evolution ( Lynch, 2007 ; Bijma, 2013 ; Fisher and Mcadam, 2019 ). Horizontal gene transfer ( Bennetzen, 1996 ) and allopolyploidy ( Abbott et al, 2013 ) are often regarded as the typical processes that lead to the interaction of various genomes within a single organism.…”

Social Selection and the Evolution of Maladaptation

“…In extreme cases, selection may decrease population mean fitness enough to lead to population extinction, a phenomenon known as “self-extinction” (Matsuda and Abrams 1994), “evolutionary suicide” (Gyllenberg and Parvinen 2001), or “Darwinian extinction” (Webb 2003). Social interactions are particularly likely to create conditions where selection leads to a decrease in fitness (Matsuda and Abrams 1994; Kokko and Brooks 2003; Fisher and McAdam 2019; Henriques and Osmond 2020). While social effects on the fitness of others may enhance adaptation when the interests of social partners are aligned (Henriques and Osmond 2020), maladaptation and even population extinction are possible when selection leads to the evolution of competitive traits that increase individual fitness at the expense of others (Wright 1969; Matsuda and Abrams 1994; Webb 2003).…”