Mating preferences of selfish sex chromosomes

The evolution of female mating preferences for harmful male traits is a central paradox of sexual selection 1 – 9 . Two dominant explanations for this paradox 8 , 10 are Fisher’s runaway process, which is based on genetic correlations between preference and trait 1 , 3 , 4 , and Zahavi’s handicap pr...

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Bibliographic Details
Published in:Nature (London) 2019-06, Vol.570 (7761), p.376-379
Main Author: Muralidhar, Pavitra
Format: Article
Language:English
Subjects:
631/181/2468
631/181/2470
631/181/2474
631/181/457
Alleles
Animal behavior
Animal reproduction
Animals
Biological evolution
Chromosomes
Evolution
Evolution, Molecular
Female
Fitness
Gene expression
Genetic research
Humanities and Social Sciences
Letter
Male
Males
Mate selection
Mating
Mating Preference, Animal
Models, Biological
Models, Genetic
multidisciplinary
Offspring
Preferences
Repetitive Sequences, Nucleic Acid - genetics
Reproductive fitness
Science
Science (multidisciplinary)
Sex
Sex chromosomes
Sex Chromosomes - genetics
Sex linkage
Sexual selection
Signal quality
Trends
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Summary:The evolution of female mating preferences for harmful male traits is a central paradox of sexual selection 1 – 9 . Two dominant explanations for this paradox 8 , 10 are Fisher’s runaway process, which is based on genetic correlations between preference and trait 1 , 3 , 4 , and Zahavi’s handicap principle, in which the trait is an honest costly signal of male quality 2 , 6 , 8 , 11 . However, both of these explanations require the exogenous initial spread of female preferences before harmful male traits can evolve 1 – 4 , 6 , 8 , 11 . Here I present a mechanism for the evolution of female mating preferences for harmful male traits that is based on the selfish evolutionary interests of sex chromosomes. I demonstrate that female-biased genetic elements—such as the W and X sex chromosomes—will evolve mating preferences for males who display traits that reduce their fitness and/or that of their male offspring, but increase fitness in female offspring. In particular, W-linked preferences can cause nearly lethal male traits to sweep to fixation. Sex-linked preferences can drive the evolution of traits such as ornamental handicaps and male parental care, and can explain variation in ornamentation and behaviour across taxa with divergent sex-determining mechanisms. Population genetic modelling shows that mate preferences encoded on sex chromosomes can drive the evolution of extremely male-costly traits.
ISSN:0028-0836
1476-4687
DOI:10.1038/s41586-019-1271-7