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Sex-specific morphs: the genetics and evolution of intra-sexual variation

Abstract

Sex-specific morphs exhibit discrete phenotypes, often including many disparate traits, that are observed in only one sex. These morphs have evolved independently in many different animals and are often associated with alternative mating strategies. The remarkable diversity of sex-specific morphs offers unique opportunities to understand the genetic basis of complex phenotypes, as the distinct nature of many morphs makes it easier to both categorize and compare genomes than for continuous traits. Sex-specific morphs also expand the study of sexual dimorphism beyond traditional bimodal comparisons of male and female averages, as they allow for a more expansive range of sexualization. Although ecological and endocrinological studies of sex-specific morphs have been advancing for some time, genomic and transcriptomic studies of morphs are far more recent. These studies reveal not only many different paths to the evolution of sex-specific morphs but also many commonalities, such as the role of sex-determining genes and hormone signalling in morph development, and the mixing of male and female traits within some morphs.

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Fig. 1: Examples of sex-specific morphs.
Fig. 2: Disruptive selection for extreme male traits results in different reproductive morphs.
Fig. 3: Allometric relationships between and within the sexes for beetle horn and body size.

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Acknowledgements

The author is grateful for current funding through a Canada 150 Research Chair, the Natural Sciences and Engineering Research Council of Canada, the Canada Foundation for Innovation and past support from the European Research Council. The author is indebted to current and past lab group members and collaborators for the rich intellectual environment they created, and thanks in particular F. Breden, B. Sandkam, B. Dean, A. Wright, S. Alonzo, D. Promislow and J. Avise for discussions about morph evolution that shaped many of the views presented. The author thanks A. Moczek, P. Rohner, A. Cordero-Rivera and F. Hendrickx for animal pictures that formed the basis of Fig. 1, and three anonymous reviewers for helpful and constructive feedback.

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Glossary

Alternative mating strategies

Different reproductive behaviours used by male or female animals. Sometimes referred to as alternative reproductive tactics.

Sexually selected traits

Traits that help to increase reproductive fitness. Somatic sexually selected traits, such as songs or bright colours, can help to attract mates, or, like antlers, can be used in male–male competition for access to mates. Gonadal sexually selected traits often relate to sperm competition after mating.

Caruncles

Fleshy tuberosities that can be present on head, neck, cheeks or throat of some birds. In the case of turkeys, caruncles include the wattle and the snood, an erectile protuberance on the forehead.

Sneaker male

A male that lacks somatic sexually selected traits and mates primarily via stealth.

Territorial males

Sometimes called bourgeois or alpha males. A male reproductive strategy that is typically associated with somatic sexually selected traits, such as bright colours and mating behaviours, to attract females to a specific defended territory or nesting site.

Helper male

Sometimes called a satellite male in birds and fish. A male morph that lacks sexually selected traits and behaviours, and which assists a territorial male in nest defence and care in exchange for a limited number of fertilization events.

Heritable

A phenotype that is at least partially transmitted genetically from parents to offspring.

Allometry

The scaling relationships between size and shape across different parts of the body.

Female mimic

Also called a gynomorph. A male morph that exhibits female somatic phenotypes.

Andromorph

Also called a male mimic, a female morph that exhibits many male somatic phenotypes.

Batesian mimics

Organisms that mimic the warning colouration of a noxious model, thereby gaining protection from predators.

Disruptive selection

A form of selection in which extreme phenotypes are more fit than intermediate forms.

Reproductive fitness

The relative ability of a genotype to pass on its genetic material to the next generation. Often measured as the proportion of offspring generated relative to other genotypes in the population.

Integrated

The tendency of different traits to vary jointly in a coordinated manner throughout a morphological structure or even a whole organism.

Sex-biased genes

Genes that are transcribed at different levels in males and females. Often thought to be a major underlying mechanism for sexually dimorphic phenotypes.

Supergenes

Chromosomal regions that encompass multiple genes that are inherited together because of close genetic linkage. Often supergenes are associated with chromosomal inversions, which prevent recombination with the alternative allele.

Isoforms

Proteins produced from the same genetic locus but which differ in exon order or combination.

Balancing selection

A form of selection in which multiple phenotypes (or alleles) are maintained in a population.

Threshold trait

A phenotype for which the variation assorts into groups instead of continuously, and for which the underlying cause is determined by a critical value.

Indeterminate growth

A form of growth that continues throughout the life of the organism, instead of stopping at a predetermined size or age.

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Mank, J.E. Sex-specific morphs: the genetics and evolution of intra-sexual variation. Nat Rev Genet (2022). https://doi.org/10.1038/s41576-022-00524-2

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