Haldane's rule
Haldane's rule represents one of the most phenomenal observations in early speciation. It was formulated in 1922 by the British evolutionary biologist J.B.S. Haldane:
“When in the offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous (heterogametic) sex”. [1]
Haldane’s rule applies to the vast majority of heterogametic organisms examined. These include both male heterogametic (XY or XO-type sex determination, such as mammal and Drosophila) and female heterogametic (ZW-type sex determination, such as birds and Lepidoptera) animals, and even dioecious plants (such as poplar tree). It appears to be a general pattern of speciation that is associated with heterogamety.
The fact that evolution can produce such a consistent pattern of isolation in a vast array of different organisms is striking. However, the actual mechanism(s) leading to this consistency in broad taxa appears to be rather complicated. The mechanistic basis by which the heterogametic sex becomes more susceptible to hybrid inferiority (sterility or inviability) has been a focus of theoretical and empirical explorations that have greatly enriched our understanding of sexual reproduction and speciation.
Many different hypotheses have been advanced to explain the cause of Haldane's rule. Most hypotheses equal the genetic basis to the cause of Haldane’s rule. Currently, the most popular explanation for Haldane’s rule is the composite hypothesis. The composite hypothesis divides Haldane’s rule into multiple subdivisions, including sterility, inviability, male heterogamety and female heterogamety. The composite hypothesis believes that Haldane’s rule in different subdivisions have different causes. Individual genetic mechanisms may not be mutually exclusive and these mechanisms might act together to cause Haldane’s rule in any given subdivision.[2][3] In contrast to these views that emphasize on the genetic bases, another view hypothesizes that the population dynamics during population divergence may cause Haldane’s rule.[4] The following are the main hypotheses,
- The dominance hypothesis: Heterogametic hybrids are affected by all, recessive and dominant, X-linked genes involved in incompatibilities, while homogametic hybrids are only affected by the dominant ones. The X-linked incompatibility between diverging populations is more likely displayed in the heterogametic sex than homogametic sex.
- The faster male hypothesis: Male genes evolve faster due to sexual selection. As a result, male sterility becomes more prominent in male heterogametic taxa (XY sex determination). This hypothesis contradicts with Haldane’s rule in homogametic taxa, in which females are more affected. It therefore only applies to a subdivision, sterility in taxa with XY sex determination, according to the composite theory.
- Meiotic drive: In hybrid populations, selfish genetic elements inactivate sperm cells (i.e.: an X-linked drive factor inactivates a Y-bearing sperm and vice versa).
- Faster X theory: X-linked have a larger effect in reproductive isolation.
- Differential selection theory: Hybrid incompatibilities affecting the heterogametic sex and homogametic sex are fundamentally different isolating mechanisms, which makes heterogametic inferiority (sterility/inviability) more visible or preserved in nature.
Data from multiple phylogenetic groups support a "dominance and faster X–chromosome" theory [5].
The dominance hypothesis is the core of the composite theory and the X-linked recessive/dominance effects have been demonstrated in many cases to cause hybrid incompatibilities. There is also supporting evidence for the faster male hypothesis and meiotic drive hypothesis. For example, a significant reduction of male-driven gene flow is observed in Asian elephants, suggesting a faster evolution of male traits.[6]
Haldane's rule has a correspondence with the observation that some negative recessive genes are sex-linked and express themselves more often in men than women, such as color blindness or haemophilia.
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 species lacking chromosomal sex determination, such as haplodiploids.[7]
[edit] Exceptions
There are notable exceptions to Haldane's rules where the homogametic sex turns out to be unviable while the heterogametic sex is viable and fertile. This has been most commonly noted in Drosophila,[8] where it is proposed to function through maternal effect genes, and their interaction with species specific heterochromatin.[9]
[edit] References
- ^ Haldane, J. B. S. (1922). "Sex ratio and unisexual sterility in hybrid animals". J. Genet. 12: 101–109. doi:10.1007/BF02983075.
- ^ Orr, H. A. (1993). "Haldane's rule has multiple genetic causes". Nature 361 (6412): 532–533. doi:10.1038/361532a0. PMID 8429905. http://www.nature.com/nature/journal/v361/n6412/pdf/361532a0.pdf.
- ^ 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. doi:10.1086/285534. PMID 19425975. http://www.jstor.org/stable/pdfplus/2462812.pdf?acceptTC=true.
- ^ 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. doi:10.1046/j.1420-9101.2003.00528. PMID 14635874. http://onlinelibrary.wiley.com/doi/10.1046/j.1420-9101.2003.00528.x/pdf.
- ^ M. Schilthuizen, M. C. Giesbers and L. W. Beukeboom. (2011). Haldane's rule in the 21st century. Heredity10.1038/hdy.2010.170
- ^ Fickel, J.; Lieckfeldt, D.; Ratanakorn, P.; Pitra, C. (2007). "Distribution of haplotypes and microsatellite alleles among Asian elephants (Elephas maximus) in Thailand". European Journal of Wildlife Research 53 (4): 298–303. doi:10.1007/s10344-007-0099-x. http://www.springerlink.com/index/R0Q2143R8852824N.pdf. Retrieved 2008-04-14.
- ^ Koevoets T; Beukeboom LW. (2009). "Genetics of postzygotic isolation and Haldane's rule in haplodiploids.". Heredity 102 (1): 16–23. doi:10.1038/hdy.2008.44. PMID 18523445. http://www.nature.com/hdy/journal/v102/n1/abs/hdy200844a.html. Retrieved 2009-11-04.
- ^ Sawamura K. (1996). "Maternal effect as a cause of exceptions for Haldane's rule.". Genetics 143 (1): 609–611. PMC 1207293. PMID 8722809. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=1207293. Retrieved 2009-11-04.
- ^ 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. doi:10.1371/journal.pbio.1000234. PMC 2760206. PMID 19859525. http://www.plosbiology.org/article/info%3Adoi%2F10.1371%2Fjournal.pbio.1000234. Retrieved 2009-11-04.
[edit] Other references
- Coyne, J.A. (1985): The genetic basis of Haldane's rule. Nature 314(6013): :736–738. Retrieved 2007-JAN-26. NCBI Pubmed Abstract.
- Forsdyke, Donald (2005): Haldane's rule. Version of 2005-DEC-6. Retrieved 2006-OCT-11.
- Naisbit, Russell E.; Jiggins, Chris D.; Linares, Mauricio; Salazar, Camilo; Mallet, James (2002). "Hybrid Sterility, Haldane's Rule and Speciation in Heliconius cydno and H. melpomene". Genetics 161 (4): 1517–1526. PMC 1462209. PMID 12196397. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool=pmcentrez&artid=1462209.
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