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Review
. 2014 Jul 1;12(7):e1001899.
doi: 10.1371/journal.pbio.1001899. eCollection 2014 Jul.

Sex determination: why so many ways of doing it?

Doris Bachtrog  1 , Judith E Mank  2 , Catherine L Peichel  3 , Mark Kirkpatrick  4 , Sarah P Otto  5 , Tia-Lynn Ashman  6 , Matthew W Hahn  7 , Jun Kitano  8 , Itay Mayrose  9 , Ray Ming  10 , Nicolas Perrin  11 , Laura Ross  12 , Nicole Valenzuela  13 , Jana C Vamosi  14 ; Tree of Sex Consortium
Affiliations
Review

Sex determination: why so many ways of doing it?

Doris Bachtrog et al. PLoS Biol. .

Abstract

Sexual reproduction is an ancient feature of life on earth, and the familiar X and Y chromosomes in humans and other model species have led to the impression that sex determination mechanisms are old and conserved. In fact, males and females are determined by diverse mechanisms that evolve rapidly in many taxa. Yet this diversity in primary sex-determining signals is coupled with conserved molecular pathways that trigger male or female development. Conflicting selection on different parts of the genome and on the two sexes may drive many of these transitions, but few systems with rapid turnover of sex determination mechanisms have been rigorously studied. Here we survey our current understanding of how and why sex determination evolves in animals and plants and identify important gaps in our knowledge that present exciting research opportunities to characterize the evolutionary forces and molecular pathways underlying the evolution of sex determination.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Sex chromosome differentiation.
A. Reconstructed evolutionary path of sex chromosome differentiation in humans. Sex chromosomes originate from autosomes that acquired a sex-determining function (the Sry gene) after their split from monotremes. Suppression of recombination between the sex chromosomes, associated with degeneration of the non-recombining region of the Y chromosome, results in the morphological and genetic differentiation of sex chromosomes. Recombination suppression occurred in multiple episodes along the human X and Y chromosome, forming so-called evolutionary strata. The oldest stratum is shared between eutherian mammals and marsupials, while the youngest stratum of humans is primate-specific. B. The degree of sex chromosome differentiation ranges widely across species, spanning the entire spectrum of homomorphic to heteromorphic sex chromosomes, from a single sex-determining locus, as seen in pufferfish, a small differentiated region (strawberry and emu), most of the sex chromosomes apart from short recombining regions (humans), to the entire sex chromosome pair, as seen in Drosophila. Note that the sex chromosomes are not drawn to scale.
Figure 2
Figure 2. Evolutionary pathways from hermaphroditism to separate sexes.
Shown are two-step pathways involving intermediate male- and female-sterile individuals. Loss-of-function mutations (red) are assumed to be recessive, while gain-of-function mutations (green) are assumed to be dominant. Ancestral alleles are in black. M, male fertility allele; m, male sterility mutation; F, female fertility allele; f, female sterility mutation. Because loss of function mutations (red) are almost 50 times more frequent than gain of function mutations (green) in flowering plants, we would expect pathways 1 (e.g., some poplar species) or 2 (e.g., papaya) to arise earlier. Furthermore, transitions through gynodioecy, pathways 2 and 3 (e.g., strawberry) allow females to completely avoid inbreeding depression, while transitions through androdioecy are more costly because males must compete with hermaphrodites for fertilization and do not have any of their own ovules to fertilize. These theoretical arguments help to account for the prevalence of gynodioecy and the XY chromosome system (via pathway 2) observed in plants; nevertheless, all four pathways may be biologically relevant, although no known examples for pathway 4 currently exist.
Figure 3
Figure 3. Diversity of sex determination systems for representative plant and animal clades.
The bubble insert graph for the plant clades represents the relative proportion of species with documented sex chromosomes within plants with separate sexes. Vertebrates: Mammalia (placental, marsupial, and monotreme mammals), Aves (birds), Reptilia (turtles, snakes, crocodiles, lizards), Amphibia (frogs, toads, salamanders), and Teleostei (bony fishes). Invertebrates: Acari (mites and ticks), Crustacea (shrimps, barnacles, crabs), and Insects, which include Coccoidea (scale insects), Coleoptera (beetles), Hymenoptera (ants, bees, and wasps), Lepidoptera (butterflies), and Diptera (flies). Plants: Gymnosperms (non-flowering plants) and Angiosperms (flowering plants).
Figure 4
Figure 4. Schematic overview of some sex determination (SD) mechanisms.
M refers to meiosis, F to fertilization. Haploid stages (n) are indicated as shaded areas and diploid stages (nn) are unshaded. Hermaphrodites: Most flowering plants (and gastropods and earthworms) simultaneously contain both male and female sexual organs (simultaneous hermaphrodites). Many fish and some gastropods and plants are sequential hermaphrodites; clownfish, for example, are born males and change into females, while many wrasses or gobies begin life as females and then change to males. Environmental Sex Determination: In turtles and some other reptiles, sex is determined by incubation temperature of the eggs (temperature-dependent sex determination). Social factors can act as primary sex-determining cues: sexually undifferentiated larvae of the marine green spoonworm that land on unoccupied sea floor develop into females (and grow up to 15 cm long), while larvae that come into contact with females develop into tiny males (1–3 mm long) that live inside the female. Genotypic Sex Determination: Almost all mammals and beetles, many flies and some fish have male heterogamety (XY sex chromosomes), while female heterogamety (ZW sex chromosomes) occurs in birds, snakes, butterflies, and some fish. In mosses or liverworts, separate sexes are only found in the haploid phase of the life cycle of an individual (UV sex chromosomes). In some flowering plants and fish, such as zebrafish, sex is determined by multiple genes (polygenic sex determination). In bees, ants, and wasps, males develop from unfertilized haploid eggs, and females from fertilized diploid eggs (haplodiploidy), while males of many scale insects inactivate or lose their paternal chromosomes (paternal genome elimination). In some species, sex is under the control of cytoplasmic elements, such as intracellular parasites (e.g., Wolbachia) in many insects or mitochondria in many flowering plants (cytoplasmic sex determination). In some flies and crustaceans, all offspring of a particular individual female are either exclusively male or exclusively female (monogeny).
Figure 5
Figure 5. Transitions versus differentiation of sex chromosomes.
Transitions between homomorphic sex chromosomes result from new masculinizing (M′) or feminizing (F′) mutations that invade an existing XY or ZW system to create a new chromosome pair (in grey) that harbors the sex-determining gene (additional transitional karyotypes are indicated by unshaded circles). XY→XY transitions result in the loss of the ancestral Y (and ZW→ZW transitions cause loss of the ancestral W). Transitions between XY and ZW systems result in some offspring that are homozygous for the Y (blue) or W (red) chromosome and are thus more likely if the chromosomes have similar gene content but become increasingly difficult if these chromosomes have degenerated (side boxes on left and right), causing YY and WW individuals to be less fit.
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