Sexual Selection Theory and Mitonuclear Mate Choice
Over 150 years ago, Darwin proposed that male animals are ornamented because female animals are attracted to ornamentation during mate choice. This powerful insight has been corroborated in a diverse array of species of animals. The question that haunted Darwin to his deathbed remains unresolved: why do females assess ornamentation when choosing mates?
We propose that indicator traits, such as carotenoid coloration, are signals of the efficiency of OXPHOS (explained in detail in papers in Integrative and Comparative Biology and Biological Reviews cited below). Indeed the oxidation of carotenoids into ornamental pigments is intimately linked to mitochondrial function (Hill and Johnson 2012, Johnson and Hill 2013). This observation potentially explains the many ornamental traits for which the expression has been linked to condition. This Index Hypothesis is explained in a recent paper for which my former student Ryan Weaver was lead author (Weaver et al. 2017).
We are working on a new theory to explain the evolution of ornamental traits. In a recent theoretical sketch (Hill and Johnson 2013) we hypothesized that it is the need for females to locate mates with nuclear genes that will express in mitochondria (N-mt genes) that are compatible with her mitochondrial genes (mt genes) that has driven the evolution of female choice for ornamental traits. The products of N-mt and mt genes form complexes in the mitocondria that enable oxidative phosphorylation (OXPHOS) and hence that are responsible for energy production. Any incompatibility between N-mt and mt genes will lead to reduced energy efficiency and loss of functionality.
Females seek information about three basic aspects of propsective mates: quality, species identity, and sexiness (Hill 2018). For a female to properly assess mitonuclear compatibility in males via ornamentaion, those prospective mates must share a functional mitotype with the choosing female. Because of the need for mitonuclear compatibility, there tends to be little or no variation in functional mitotypes within populations (species), so females should be selected to recognize species boundaries. Hence, we propose that the species-typical ornamentation seen in some animals are signals of species identity (Hill 2015). The Fisher/Kirkpatrick/Lande model proposes that the inherent beauty (sexiness) of an ornament can lead to its elaboration. At present, this runaway process is the only explanation for highly elaborate traits, but it does not fit empirical observations very well (Koch and Hill 2015).
Key recent citations related to sexual selection and mate choice from the Hill Lab:
Powers, M. J. and Hill, G. E. 2021. A review and assessment of the Shared-Pathway Hypothesis for the maintenance of signal honesty in red ketocarotenoid-based coloration. Integrative and Comparative Biology. doi.org/10.1093/icb/icab056
Powers, M. J., Hill, G. E., and Weaver, R. J. 2019. An experimental test of mate choice for red carotenoid coloration in the marine copepod, Tigriopus Californicus. Ethology DOI: 10.1111/eth.12976.
Powers, M. J., Wilson, A. E., Heine, K. B., and Hill, G. E. 2020. The relative importance of various mating criteria in copepods. Journal of Plankton Research 42: 19–30.
Hill, G.E., 2018. Mitonuclear Mate Choice: A Missing Component of Sexual Selection Theory?. BioEssays, 40(3), p.1700191.
Weaver, R. J., R. E. Koch, and G. E. Hill. 2017. What maintains signal honesty in animal color displays used in mate choice? Phil. Trans. Roy. Soc. Lond.
Koch, R.E., C.J. Josefson, and G.E. Hill. 2016. Mitochondrial function, ornamentation, and immunocompetence. Biological Reviews. http://onlinelibrary.wiley.com/doi/10.1111/brv.12291/abstract
Koch, R. E. and G. E. Hill. 2015. A millennium of stasis in avian ornamentation? Implications for sexual selection theory.Ideas in Ecology and Evolution 8:70-75.
Hill, G. E. 2015. Selection for reinforcement versus selection for signals of quality and attractiveness. Ideas in Ecology and Evolution 8:67-69.
Hill. G. E. 2015. Sexiness, individual condition, and species identity: the characteristics of prospective mates signaled by ornamentation. Evolutionary Biology 42 (3) 251-259.
Koch R. and Hill, G. E. 2015. Rapid evolution of bright monochromatism in the domestic Atlantic Canary (Serinus canaria). Wilson Journal of Ornithology 127(4):615-621.
Hill, G. E. 2015. Mitonuclear Ecology. Molecular Biology and Evolution. doi: 10.1093/molbev/msv104
Hill. G. E. 2014. Sex linkage of nuclear-encoded mitochondrial genes. Heredity 112, 469–470
Hill, G. E. 2014. Cellular Respiration: The Nexus of Stress, Condition, and Ornamentation. Integrative and comparative biology 54:.645-657.
Hill, G. E. and Johnson, J. D. 2013. The mitonuclear compatibility hypothesis of sexual selection. Proceedings of the Royal Society of London, B.