The widespread presumption that inbreeding depression will inevitably cause net selection for inbreeding avoidance ignores the inclusive fitness benefit of inbreeding that exists because parents are more closely related to inbred offspring than to outbred offspring. This increased relatedness arises because inbred offspring, by definition, inherit alleles from one parent that are identical by descent to those carried by, and potentially inherited from, the other parent. Inbreeding thereby increases the expected proportion of alleles that any one parent shares with its offspring, including alleles favouring inbreeding [10,24,25]. This inclusive fitness benefit underpins extensive theory predicting the evolution of self-fertilisation in plants [10,25–27]. That this same benefit could also cause the evolution of biparental inbreeding was suggested three decades ago (Box 1) [28,29], but remained widely ignored by animal ecologists. The assumption that inbreeding depression inevitably causes selection for inbreeding avoidance continued to pervade hypotheses explaining dispersal, mate choice, and polyandry [3,5,6,11,30–32]. Recent theory has re-emphasised that biparental inbreeding could be adaptive, even given inbreeding depression, with the inclusive fitness benefit phrased as ‘helping relatives to breed’ and hence kin selection [12,13,33].What Happens after Inbreeding Avoidance? Inbreeding by Rejected Relatives and the Inclusive Fitness Benefit of Inbreeding Avoidance
The fitness costs associated with inbreeding, primarily inbreeding depression in resulting offspring, have caused a widespread assumption among animal ecologists that inbreeding avoidance must be adaptive [10, 21, 22]. Meanwhile, empirical studies have reported a lack of inbreeding avoidance [34, 42–47], or even an apparent preference for inbreeding [48–52], causing a mismatch between expectations and data . This mismatch is partially resolved by basic conceptual models of biparental inbreeding that imply that the inclusive fitness benefit of inbreeding might cause inbreeding tolerance or preference to be adaptive even given inbreeding depression in offspring fitness, and that predict sexual conflict over inbreeding [24–28]. [. . .]Related:
Our models imply that the inclusive fitness costs and benefits of inbreeding versus avoiding inbreeding will vary among individuals depending on their interactions with multiple different relatives of both sexes, and on the degree to which focal individuals are themselves inbred. Understanding these costs and benefits and their combined consequences for the evolution of inbreeding strategies therefore requires consideration of not only the relatedness of an individual to its potential mate(s), but also the relatedness between the individual and the subsequent mates of rejected relatives. Knowledge of the distribution of relatedness within a population is therefore likely to be critical for understanding the evolution of inbreeding strategies. This distribution will in turn depend on the distribution of relatedness in previous generations and on previously realised inbreeding strategies and inbreeding loads, thereby generating complex feedbacks between inbreeding strategy, load, and relatedness. [. . .]
Sexual conflict and interactions among multiple non-self relatives are particular to biparental reproduction rather than self-fertilisation, but both types of inbreeding increase the expression of inbreeding load causing inbreeding depression in offspring [1, 2, 7, 12]. Inbreeding depression may decrease inbreeding load by exposing deleterious homozygous recessive alleles to selection [9, 71]. Resulting purging of deleterious recessive alleles may in turn affect the inclusive fitness benefit of inbreeding versus avoiding inbreeding causing inbreeding strategy and inbreeding load to coevolve [12, 72, 73]. The consequences of this coevolution have been modelled extensively with respect to outcrossing versus selfing [12, 18, 72, 74–76], but have not yet been modelled for the evolution of biparental inbreeding strategies . Future theoretical developments will therefore need to explicitly consider coevolution between biparental inbreeding strategy and inbreeding load.
Predictive models of biparental inbreeding evolution cannot be simple, but their complexity need not preclude generality . Tractable approaches for developing inbreeding theory might include game-theoretic models, or individual-based models that explicitly track ancestry and inbreeding load, and thereby incorporate feedbacks among relatedness, load, and inbreeding strategy.