The evolution of costly mate choice against segregation distorters

Abstract

The evolution of female preference for male genetic quality remains a controversial topic in sexual selection research. One well-known problem, known as the lek paradox, lies in understanding how variation in genetic quality is maintained in spite of natural selection and sexual selection against low-quality alleles. Here, we theoretically investigate a scenario where females pay a direct fitness cost to avoid males carrying an autosomal segregation distorter. We show that preference evolution is greatly facilitated under such circumstances. Because the distorter is transmitted in a non-Mendelian fashion, it can be maintained in the population despite directional sexual selection. The preference helps females avoid fitness costs associated with the distorter. Interestingly, we find that preference evolution is limited if the choice allele induces a very strong preference or if distortion is very strong. Moreover, the preference can only persist in the presence of a signal that reliably indicates a male's distorter genotype. Hence, even in a system where the lek paradox does not play a major role, costly preferences can only spread under specific circumstances. We discuss the importance of distorter systems for the evolution of costly female choice and potential implications for the use of artificial distorters in pest control.

Resistance to natural and synthetic gene drive systems

“…One of the best‐known ideas is that noncarriers may avoid drive carriers as mates, preventing offspring from inheriting harmful drivers and improving offspring fitness. Theoretical models support this idea (Lande & Wilkinson, 1999; Manser et al., 2017; Randerson et al., 2000; Reinhold et al., 1999). However, this requires a trait that reliably reveals the presence or absence of drive (Lande & Wilkinson, 1999; Manser et al., 2017).…”

“…Theoretical models support this idea (Lande & Wilkinson, 1999; Manser et al., 2017; Randerson et al., 2000; Reinhold et al., 1999). However, this requires a trait that reliably reveals the presence or absence of drive (Lande & Wilkinson, 1999; Manser et al., 2017). Evidence of mate avoidance of drive carriers is weak or absent from the majority of systems studied.…”

Selfish genes and sexual selection: the impact of genomic parasites on host reproduction

“…It is interesting to note that in the stalk‐eyed flies there is evidence of a tight linkage between the preference alleles and sex ratio drive (Johns, Wolfenbarger & Wilkinson, 2005). A recent theoretical model also shows that preference can only persist in the presence of a cue that reliably indicates a male's distorter genotype (Manser, Lindholm & Weissing, 2017). We may therefore predict that selfish endosymbionts are more likely to have an effect on mate choice than other SGEs, as there is scope for these bacteria to have a direct impact on both odour production and invading the central nervous system of their host where cue processing takes place.…”

Fitness consequences of the selfish supergene Segregation Distorter

“…For this reason, it has been proposed that natural or artificially-created segregation distorters be used to spread human-beneficial alleles through wild populations, for example to introduce malaria resistance alleles into mosquitos (Gantz et al 2015). In addition to their promise for applied science, the study of segregation distorters has led to multiple advances in our understanding of evolution, genetics, and speciation (Rice 2013;Lindholm et al 2016;Manser et al 2017;Lin et al 2018;Verspoor et al 2018).…”

“…For this reason, it has been proposed that natural or artificially created segregation distorters be used to spread human‐beneficial alleles through wild populations, for example to introduce malaria resistance alleles into mosquitos (Gantz et al, ). In addition to their promise for applied science, the study of segregation distorters has led to multiple advances in our understanding of evolution, genetics and speciation (Lin et al, ; Lindholm et al, ; Manser, Lindholm, & Weissing, ; Rice, ; Verspoor, Smith, Mannion, Hurst, & Price, ). The best‐studied naturally occurring distorters are the t allele in mice (Carroll & Potts, ) and the Segregation Distorter ( SD ) allele of Drosophila melanogaster (Larracuente & Presgraves, ), both of which cause biased tranmission in heterozygous males by preventing the development of sperm that do not carry the distorter.…”