Sperm competition can drive a male-biased mutation rate

Abstract

A pattern of male-biased mutation has been found in a wide range of species. The standard explanation for this bias is that there are greater numbers of mitotic cell divisions in the history of the average sperm, compared to the average egg, and that mutations typically result from errors made during replication. However, this fails to provide an ultimate evolutionary explanation for why the male germline would tolerate more mutations that are typically deleterious. One possibility is that if there is a tradeoff between producing large numbers of sperm and expending energetic resources in maintaining a lower mutation rate, sperm competition would select for males that produce larger numbers of sperm despite a higher resulting mutation rate. Here I describe a model that jointly considers the fitness consequences of deleterious mutation and mating success in the face of sperm competition. I show that a moderate level of sperm competition can account for the observation that the male germline tolerates a higher mutation rate than the female germline.

The evolutionary ecology of testicular function: size isn't everything

“…This risk may nevertheless have to be tolerated, owing to the need to achieve high rates of sperm production under sperm competition (Blumenstiel, 2007), and it has been argued that this is an important source of male-biased mutation (Bartosch-Härlid et al, 2003;Ellegren, 2007). The limited data available testing whether life-history parameters, such as rates of extra-pair paternity or relative investment in sperm production, predict the degree of male mutation bias have so far provided mixed results.…”

Intralocus sexual conflict resolved through gene duplication

“…Significantly, most of these duplicated genes are X-to-autosome or autosome-to-autosome copies and encode for proteins with energy-production functions, while nuclear genes encoding for other mitochondrial functions (e.g., transcription, translation, and biosynthesis) remain in the genome mostly as single, broadly expressed, copies [11]. Gallach et al [11] suggested that, because sperm have a short life span and will not transfer their mitochondria to the next generation [12], natural selection might favor males which produce large amounts of sperm, or fast sperm, despite the high mutation rate that might be associated with high-energy production [13]. Therefore, while it could be beneficial to decrease the mutation rate in other tissues (i.e., soma and ovary) by preventing the formation of reactive molecules, in the case of sperm, there might be a higher benefit obtained from producing a lot of energy for fertilization, despite the mutations associated with this.…”

Do Variations in Substitution Rates and Male Mutation Bias Correlate With Life-History Traits? A Study of 32 Mammalian Genomes

“…Further, the fact that species with long generation time are also usually large has made it challenging to disentangle the effects of metabolic rate versus generation time on substitution rate (Herreid 1964; Martin and Palumbi 1993; Mooers and Harvey 1994; Speakman 2005). Third, theory suggests that increased sperm competition may occur at the expense of a higher mutation rate, leading to a higher substitution rate in species with stronger sperm competition (Blumenstiel 2007), but a study of synonymous substitution rates in six primate lineages did not have the power to detect any clear trends (Wong 2010). This progress notwithstanding, interspecies variation in substitution rates has not been studied for a large number of mammals on a genome‐wide scale.…”