Population Bottlenecks Increase Additive Genetic Variance But Do Not Break a Selection Limit in Rain Forest Drosophila

Abstract

According to neutral quantitative genetic theory, population bottlenecks are expected to decrease standing levels of additive genetic variance of quantitative traits. However, some empirical and theoretical results suggest that, if nonadditive genetic effects influence the trait, bottlenecks may actually increase additive genetic variance. This has been an important issue in conservation genetics where it has been suggested that small population size might actually experience an increase rather than a decrease in the rate of adaptation. Here we test if bottlenecks can break a selection limit for desiccation resistance in the rain forest-restricted fly Drosophila bunnanda. After one generation of single-pair mating, additive genetic variance for desiccation resistance increased to a significant level, on average higher than for the control lines. Line crosses revealed that both dominance and epistatic effects were responsible for the divergence in desiccation resistance between the original control and a bottlenecked line exhibiting increased additive genetic variance for desiccation resistance. However, when bottlenecked lines were selected for increased desiccation resistance, there was only a small shift in resistance, much less than predicted by the released additive genetic variance. The small selection response in the bottlenecked lines was no greater than that observed in the control lines. Thus bottlenecks might produce a statistically detectable change in additive genetic variance but this change has no impact on the response to selection.

Conservation genetics of population bottlenecks: the role of chance, selection, and history

“…For example, Brewer et al (1990) found no correlation between the severity of inbreeding depression and the initial genetic diversity of mice population stocks. Increases in variance following bottlenecks have also been reported in Musca domestica (Bryant et al 1986;Bryant and Meffert 1993), Drosophila melanogaster (López-Fanjul and Villaverde 1989; García et al 1994;Van Heerwaarden et al 2008) and Tribolium castaneum (Fernández et al 1995;Wade et al 1996).…”

The other 96%: Can neglected sources of fitness variation offer new insights into adaptation to global change?

“…This is essentially because such effects are most influential in small, subdivided populations incurring strong selection (Wade, 2002), which are increasingly associated with global change (Gienapp et al., 2008; Jump & Penuelas, 2005; Moller, Rubolini, & Lehikoinen, 2008). Warming‐driven declines in population size, for example, could see greater conversion of nonadditive variance into additive variance (Barton & Turelli, 2004; Cheverud et al., 1999; Goodnight, 1988; Wang et al., 1998), although van Heerwaarden, Willi, Kristensen, and Hoffmann (2008) showed that increases in the latter during population bottlenecks do not necessarily improve adaptive capacity in Drosophila . Alternatively, greater expression of nonadditive genetic effects under warming might not only hinder adaptive capacity by masking favorable or unfavorable alleles from selection, but also hinder the erosion of additive genetic variance in doing so (Crnokrak & Roff, 1995).…”

“…While our goal here was to draw attention to the size and environmental sensitivity of these effects, our work now highlights the need to better incorporate them into predictions of population persistence in changing environments. In particular, there is pressing need for studies that examine the stability of nonadditive genetic and maternal environmental effects across multiple generations (e.g., Dey et al., 2016; van Heerwaarden et al., 2008), that incorporate them into projections of population dynamics (e.g., Coulson, Tuljapurkar, & Childs, 2010), and that consider their effects in multiple or fluctuating environments. Such work is currently rare, but will enhance our ability to forecast the adaptive capacity of populations exposed to global change so they can be managed more efficiently.…”

Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences

“…Additionally, theoretical models demonstrate that genetic bottlenecks have the capacity to increase additive genetic variation in affected populations -either by "converting" epistatic into additive variation via the fixation of some alleles due to drift (Goodnight 1988) or by increasing the frequency of rare recessive alleles at loci where dominance effects occur (Robertson 1952;Willis and Orr 1993). While some studies are consistent with such predictions (Bryant and Meffert 1993; Saccheri et al 2006), on the whole empirical evidence has been equivocal (van Heerwaarden et al 2008;Jarvis 2011;Dlugosch et al 2015) and primarily derived from limited laboratory studies.…”