No evidence for short‐term purging benefits of sexual selection in inbred red flour beetle populations

Abstract

Sexual selection may increase population‐level fitness by facilitating the removal of deleterious mutations with pleiotropic effects on competition for fertilizations as well as other fitness components in both sexes. Under inbreeding, this could promote purging selection, that is the removal of deleterious recessive alleles exposed in homozygotes via matings between closely related individuals. Here, in two independent experiments, we found no evidence for short‐term purging of the inbreeding load from severely bottlenecked populations of red flour beetles, Tribolium castaneum. We hypothesize that sexual selection may have dual effects on purging, corresponding to good‐genes versus compatible‐genes mechanisms. Whereas the former should facilitate the removal of inbreeding load from bottlenecked populations, the latter may actually hamper this process while simultaneously limiting inbreeding depression by preventing the expression of deleterious recessives.

Tribolium beetles as a model system in evolution and ecology

“…However, subsequent studies using alternative approaches to examine the relationship between sexual selection and mutation load have found no purging effects (e.g. Prokop et al 2019 ). A population history (up to ten years) of experimentally applied, strong sexual selection has also been shown to improve the competitive ability of males and their sperm, and drive sperm morphology evolution (Michalczyk et al 2011 ; Demont et al 2014 ; Godwin et al 2017 ), increase conspecific population invasion success (Godwin et al 2018 ), enable population resilience to the extinction vortex (Godwin et al 2020 ), and increase the rate of pesticide resistance evolution (Jacomb et al 2016 ).…”

Environmental variance in male mating success modulates the positive versus negative impacts of sexual selection on genetic load

“…Consequently, sexual selection could potentially contribute to facilitating the evolutionary rescue of declining populations. However, in practice, the realized consequences of sexual selection for population persistence will fundamentally depend on how multiple interacting genetic processes are affected by the increased variance in male reproductive success that results from sexual selection (Holman & Kokko, 2013;Jarzebowska & Radwan, 2010;Martínez-Ruiz & Knell, 2017;Prokop et al, 2019;Singh & Agrawal, 2022;Whitlock & Agrawal, 2009). Sexual selection's expected positive effects on population fitness require that mating and/or fertilization success positively covary with fitness components that determine population growth rate (i.e.…”

“…Accordingly, considerable empirical work has tested whether sexual selection in males can indeed increase selection against deleterious mutations and thereby aid population persistence (Cally et al, 2019;Rowe & Rundle, 2021). Results are mixed: some experimental studies on a variety of species, for example, the fruit fly Drosophila melanogaster or the bulb mite Rhizoglyphus robini, report positive effects of sexual selection on population fitness (Almbro & Simmons, 2014;Godwin et al, 2020;Grieshop et al, 2016;Hollis et al, 2009;Jarzebowska & Radwan, 2010;Lumley et al, 2015;Parrett et al, 2022;Radwan, 2004), while other studies in the same or similar species did not find such effects (Allen et al, 2017;Arbuthnott & Rundle, 2012;Chenoweth et al, 2015;Hollis & Houle, 2011;Plesnar-Bielak et al, 2011Prokop et al, 2019).…”

Does operational sex ratio influence relative strength of purging selection in males versus females?

“…A classical way of testing the potential of selection in males to reduce mutation load is comparing mutation accumulation or purging between populations with different levels of sexual selection (e.g. Radwan, 2004;Hollis & Houle, 2011;Plesnar, Konior, & Radwan, 2011;Power & Holman, 2015;Prokop et al, 2019;see Table S1 for a full list of references). This is usually achieved by artificially eliminating or relaxing sexual selection in some populations, while letting it operate in others.…”