An evolutionary perspective on contemporary genetic load in threatened species to inform future conservation efforts

Abstract

In theory, genomic erosion can be reduced in fragile “recipient” populations by translocating individuals from genetically diverse “donor” populations. However, recent simulation studies have argued that such translocations can, in principle, serve as a conduit for new deleterious mutations to enter recipient populations. A reduction in evolutionary fitness is associated with a higher load of deleterious mutations and thus, a better understanding of evolutionary processes driving the empirical distribution of deleterious mutations is crucial. Here, we show that genetic load is evolutionarily dynamic in nature and that demographic history greatly influences the distribution of deleterious mutations over time. Our analyses, based on both demographically explicit simulations as well as whole genome sequences of potential donor-recipient pairs of Montezuma Quail (Cyrtonyx montezumae) populations, indicate that all populations tend to lose deleterious mutations during bottlenecks, but that genetic purging is pronounced in smaller populations with stronger bottlenecks. Despite carrying relatively fewer deleterious mutations, we demonstrate how small, isolated populations are more likely to suffer inbreeding depression as deleterious mutations that escape purging are homogenized due to drift, inbreeding, and ineffective purifying selection. We apply a population genomics framework to showcase how the phylogeography and historical demography of a given species can enlighten genetic rescue efforts. Our data suggest that small, inbred populations should benefit the most when assisted gene flow stems from genetically diverse donor populations that have the lowest proportion of deleterious mutations.

Genetic load: genomic estimates and applications in non-model animals

“…In diploid organisms, the genetic load can be partitioned into the realized load (also known as expressed load 6 ) and the masked load (also known as the inbreeding load 15,16 or potential load 17,18 ). The realized load reduces the fitness in the current generation, whereas the masked load quantifies the potential fitness loss due to (partially) recessive deleterious mutations that may become expressed in future generations depending on the population's demography (for example, inbreeding, population decline or subdivision).…”

“…2). Consequently, even after demographic recovery, migration or genetic rescue might be required to replace fixed deleterious variants and restore fitness 18 .…”

“…During population decline, part of this load is lost by random genetic drift, and part is purged by selection as recessive deleterious mutations with large fitness effects become exposed by inbreeding 53,56,94 . However, a proportion of the masked load is converted into realized load, resulting in inbreeding depression 18 . Both the type of demographic contraction and the distribution of the fitness effects of mutations play important roles in determining these processes 10,21 .…”

“…Harmful variants can become fixed during extreme bottlenecks, but those with larger fitness effects are likely to be purged during longterm declines 56,67,[95][96][97][98][99] . Persistently small, isolated populations are expected to exhibit increased load accumulation due to strong genetic drift 18,59,62,64 . In this case, highly harmful mutations might be effectively purged when exposed to selection under most conditions, but mildly deleterious variants can accumulate during demographic collapse 22,100 (Fig.…”

Genomic consequences of a century of inbreeding and isolation in the Danish wild boar population

“…Here, we illustrate that despite an extreme founder effect, the population appears viable. There is growing evidence that after an initial bottleneck, small populations often tend to purge some of the deleterious variants (Goodnight, 1988 ; Grossen et al, 2020 ; Mathur et al, 2021 ). Various studies (Kyriazis et al, 2019 ; Robinson et al, 2018 ; van der Valk et al, 2019 ; Xue et al, 2015 ) have proposed the role of purging of highly deleterious variants in small and isolated populations as an underlying mechanisms for their persistence with low levels of genetic diversity.…”