Abstract
The molecular mechanisms that control sexual dimorphism are very different in distantly related animals. Did sex determination arise several times with different regulatory mechanisms, or is it an ancient process with little surviving evidence of ancestral genes? The recent identification of related sexual regulators in different phyla indicates that some aspects of sexual regulation might be ancient. Studies of sex-determining mechanisms are beginning to reveal how sexual dimorphism arises and evolves.
Key Points
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Sex-determining pathways in different species are initiated by a surprising variety of genetic and environmental signals.
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Sex chromosomes can evolve quickly and generally are not conserved at the molecular level, between distant species.
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Experimental manipulations of Caenorhabditis elegans show how sex-determination mechanisms can be completely transformed by simple mutations in regulatory genes.
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Comparisons of nematodes with insects indicate that sexual regulators that function upstream in the developmental hierarchy might evolve very rapidly, but that downstream genes are more highly conserved.
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Flies, worms and mammals regulate the various aspects of sexual development with genes that contain the DM-domain DNA-binding motif.
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The conservation of downstream sex-determining genes and the divergence of those upstream fits theoretical predictions.
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Sexual regulation must be integrated with spatial and temporal regulation. The control of sexual dimorphism in the posterior of flies and worms illustrates how this can occur.
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Short-range transcriptional repression seems to generate sexual dimorphism in worms, and might be a general mechanism in other species.
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Acknowledgements
The author thanks V. Bardwell, B. Charlesworth, E. Coucouvanis, J. Simon and three referees for critical reading of the manuscript; S. Carroll, A. Kopp and J. Hodgkin for sharing results before publication; and apologizes to those whose work could not be cited due to space limitations. Work in the Zarkower laboratory is supported by grants from the National Institutes of Health.
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Glossary
- BDELLOID ROTIFER
-
(or simply bdelloids, from the Greek word for leech). Microscopic aquatic animals. Most species creep on a surface by alternately moving their front and back ends, such as in an inchworm or a leech.
- HETEROGAMETIC SEX
-
The sex that produces gametes with different sex chromosomes. In XX/XY sex determination, the male is heterogametic, and in ZZ/ZW sex determination, the female is heterogametic.
- G-BANDING
-
(Giemsa banding). One of several methods for staining chromosomes, which produces light and dark bands characteristic for each homologous chromosome pair, so that individual chromosomes can be distinguished and examined for abnormalities in structure and number.
- RNA INTERFERENCE
-
(RNAi). This is a process by which double-stranded RNA specifically silences the expression of homologous genes through degradation of their cognate mRNA.
- SEX COMBS
-
Specialized rows of sensory bristles on the foreleg of male fruitflies, which are used during courtship to grip the female.
- SENSORY RAYS
-
Specialized sense organs in the nematode male tail, consisting of two sensory neurons and a structural cell. Used to locate and copulate with females.
- SERTOLI CELLS
-
Cells in the testis that produce secreted factors, including Müllerian inhibiting substance, and act as 'nurse cells' to provide nourishment to the early sperm cells.
- HOX PROTEINS
-
Transcription factors that are expressed in specific patterns, which are important for determining regional identity along the anterioposterior axis in the embryo.
- DEUTEROSTOME/PROTOSTOME
-
The two principal divisions of the animal phyla, based on how the mouth forms in the embryo.
- PLEIOTROPY
-
The phenomenon in which a single gene is responsible for several distinct and seemingly unrelated phenotypic effects.
- HYPODERMIS
-
The cellular layer that underlies and secretes the cuticle that forms the outer coating of a nematode or arthropod.
- BASIC HELIX–LOOP–HELIX
-
A common dimerization and DNA-binding motif. The helices mediate dimerization, and the adjacent basic region is required for DNA binding.
- CRYPTORCHIDISM
-
The failure of the testicles to descend from the abdominal cavity into the scrotum by one year of age (in humans).
- HETEROCHRONY
-
An evolutionary change in phenotype based on an alteration in the timing of developmental events.
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Zarkower, D. Establishing sexual dimorphism: conservation amidst diversity?. Nat Rev Genet 2, 175–185 (2001). https://doi.org/10.1038/35056032
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DOI: https://doi.org/10.1038/35056032
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