Haldane's rule

In humans, barring intersex conditions and other unusual states, it is the male that is heterogametic, with XY sex chromosomes.

Haldane's rule is an observation about the early stage of speciation, formulated in 1922 by the British evolutionary biologist J.B.S. Haldane, that states that if in a species hybrid only one sex is inviable or sterile, that sex is more likely to be the heterogametic sex. The heterogametic sex is the one with two different sex chromosomes; in mammals, for example, this is the male.[1]

Haldane himself described the rule as:

When in the F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex (heterogametic sex).[2]

Haldane's rule applies to the vast majority of heterogametic organisms. This includes the case where two species make secondary contact in an area of sympatry and form hybrids after allopatric speciation has occurred.

The rule includes both male heterogametic (XY or XO-type sex determination, such as found in mammals and Drosophila fruit flies) and female heterogametic (ZW-type sex determination, as found in birds and butterflies), and some dioecious plants such as campions.[3]

Hybrid dysfunction (sterility and inviability) is a major form of post-zygotic reproductive isolation, which occurs in early stages of speciation. Evolution can produce a similar pattern of isolation in a vast array of different organisms. However, the actual mechanisms leading to Haldane's rule in different taxa remain largely undefined.

Hypotheses

Many different hypotheses have been advanced to address the evolutionary mechanisms to produce Haldane's rule. Currently, the most popular explanation for Haldane's rule is the composite hypothesis, which divides Haldane's rule into multiple subdivisions, including sterility, inviability, male heterogamety, and female heterogamety. The composite hypothesis states that Haldane's rule in different subdivisions has different causes. Individual genetic mechanisms may not be mutually exclusive, and these mechanisms may act together to cause Haldane's rule in any given subdivision.[4][5] In contrast to these views that emphasise genetic mechanisms, another view hypothesizes that population dynamics during population divergence may cause Haldane's rule.[6]

The main genetic hypotheses are:

Data from multiple phylogenetic groups support a combination of dominance and faster X-chromosome theories.[8] However, it has recently been argued that dominance theory can not explain Haldane's rule in marsupials since both sexes experience the same incompatibilities due to paternal X-inactivation in females.[9]

The dominance hypothesis is the core of the composite theory, and X-linked recessive/dominance effects have been demonstrated in many cases to cause hybrid incompatibilities. There is also supporting evidence for the faster male and meiotic drive hypotheses. For example, a significant reduction of male-driven gene flow is observed in Asian elephants, suggesting faster evolution of male traits.[10]

Although the rule was initially stated in context of diploid organisms with chromosomal sex determination, it has recently been argued that it can be extended to certain species lacking chromosomal sex determination, such as haplodiploids[11] and hermaphrodites.[8]

Exceptions

There are notable exceptions to Haldane's rule, where the homogametic sex turns out to be inviable while the heterogametic sex is viable and fertile. This is seen in Drosophila fruit flies.[12][13]

References

  1. Turelli M, Orr HA (May 1995). "The Dominance Theory of Haldane's Rule". Genetics. 140 (1): 389–402. PMC 1206564Freely accessible. PMID 7635302.
  2. Haldane, J. B. S. (1922). "Sex ratio and unisexual sterility in hybrid animals". J. Genet. 12: 101–109. doi:10.1007/BF02983075.
  3. Brothers, Amanda N.; Delph, Lynda F. (2010). "Haldane's rule is extended to plants with sex chromosomes". Evolution. 64 (12): 3643–3648. PMID 20681984. doi:10.1111/j.1558-5646.2010.01095.x.
  4. Orr, H. A. (1993). "Haldane's rule has multiple genetic causes" (PDF). Nature. 361 (6412): 532–533. PMID 8429905. doi:10.1038/361532a0.
  5. 1 2 Wu, C.-I.; Davis, A. W. (1993). "Evolution of postmating reproductive isolation: the composite nature of Haldane's rule and its genetic bases". The American Naturalist. 142 (22): 187–212. JSTOR 2462812. PMID 19425975. doi:10.1086/285534.
  6. 1 2 Wang, R. (2003). "Differential strength of sex-biased hybrid inferiority in impeding gene flow may be a cause of Haldane's rule". Journal of Evolutionary Biology. 16 (2): 353–361. PMID 14635874. doi:10.1046/j.1420-9101.2003.00528.
  7. Charlesworth, B.; Coyne, J. A.; Barton, N. H. (1987). "The relative rates of evolution of sex chromosomes and autosomes". The American Naturalist. 130 (1): 113–146. JSTOR 10.2307/2461884. doi:10.1086/284701.
  8. 1 2 Schilthuizen, M.; Giesbers, M. C.; Beukeboom, L. W. (2011). "Haldane's rule in the 21st century". Heredity. 107 (2): 95–102. PMC 3178397Freely accessible. PMID 21224879. doi:10.1038/hdy.2010.170.
  9. Watson, E.; Demuth, J. (2012). "Haldane's rule in marsupials: what happens when both sexes are functionally hemizygous?". Journal of Heredity. 103 (3): 453–458. PMC 3331990Freely accessible. PMID 22378959. doi:10.1093/jhered/esr154.
  10. Fickel, J.; Lieckfeldt, D.; Ratanakorn, P.; Pitra, C. (2007). "Distribution of haplotypes and microsatellite alleles among Asian elephants (Elephas maximus) in Thailand" (PDF). European Journal of Wildlife Research. 53 (4): 298–303. doi:10.1007/s10344-007-0099-x.
  11. Koevoets, T.; Beukeboom, L. W. (2009). "Genetics of postzygotic isolation and Haldane's rule in haplodiploids". Heredity. 102 (1): 16–23. PMID 18523445. doi:10.1038/hdy.2008.44.
  12. Sawamura, K. (1996). "Maternal effect as a cause of exceptions for Haldane's rule". Genetics. 143 (1): 609–611. PMC 1207293Freely accessible. PMID 8722809.
  13. Ferree, Patrick M.; Barbash, Daniel A. (2009). Noor, Mohamed A. F., ed. "Species-Specific Heterochromatin Prevents Mitotic Chromosome Segregation to Cause Hybrid Lethality in Drosophila". PLOS Biology. 7 (10): e1000234. PMC 2760206Freely accessible. PMID 19859525. doi:10.1371/journal.pbio.1000234.

Further reading

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