Haldane's rule

In humans, barring intersex conditions causing aneuploidy 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 therian mammals,^[a] for example, this is the male.^[2]

Overview

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).^[3]

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 or Z0-type sex determination, as found in birds and butterflies), and some dioecious plants such as campions.^[4]

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.^[5]^[6] In contrast to these views that emphasize genetic mechanisms, another view hypothesizes that population dynamics during population divergence may cause Haldane's rule.^[7]

The main genetic hypotheses are:

Dominance: Heterogametic hybrids are affected by all X-linked alleles (be they recessive or dominant) causing incompatibilities due to divergent alleles being brought together. However, homogametic hybrids are only affected by dominant deleterious X-linked alleles. Heterogametic hybrids, which carry only a single copy of a given X-linked gene, will be affected by mutations regardless of dominance. Thus, an X-linked incompatibility between diverging populations is more likely to be expressed in the heterogametic sex than in the homogametic sex.
The "faster male": Male genes are thought to evolve faster due to sexual selection.^[6] As a result, male sterility becomes more evident in male heterogametic taxa (XY sex determination). This hypothesis conflicts with Haldane's rule in male homogametic taxa, in which females are more affected by hybrid inferiority. It therefore only applies to male 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).
The "faster X": Genes on hemizygous chromosomes may evolve more quickly by enhancing selection on possible recessive alleles causing a larger effect in reproductive isolation.^[8]
Differential selection: 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.^[7]

Data from multiple phylogenetic groups support a combination of dominance and faster X-chromosome theories.^[9] 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.^[10]

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.^[11]

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^[12] and hermaphrodites.^[9]

Exceptions

In some instances, the homogametic sex turns out to be inviable while the heterogametic sex is viable and fertile. This is seen in some Drosophila fruit flies.^[13]^[14]

Notes

^ Unlike other mammals, monotremes have more than two different sex chromosomes. The platypus has five pairs. Short-beaked echidnas have four pairs plus one female-only chromosome.^[1]

References

^ Deakin, J. E.; Graves, J. A. M.; Rens, W. (2012). "The Evolution of Marsupial and Monotreme Chromosomes". Cytogenetic and Genome Research. 137 (2–4): 113–129. doi:10.1159/000339433. hdl:1885/64794. PMID 22777195.
^ Turelli, M.; Orr, H. A. (May 1995). "The dominance theory of Haldane's rule". Genetics. 140 (1): 389–402. doi:10.1093/genetics/140.1.389. PMC 1206564. PMID 7635302.
^ Haldane, J. B. S. (1922). "Sex ratio and unisexual sterility in hybrid animals". J. Genet. 12 (2): 101–109. doi:10.1007/BF02983075. S2CID 32459333.
^ Brothers, Amanda N.; Delph, Lynda F. (2010). "Haldane's rule is extended to plants with sex chromosomes". Evolution. 64 (12): 3643–3648. doi:10.1111/j.1558-5646.2010.01095.x. PMID 20681984. S2CID 27145478.
^ Orr, H. A. (1993). "Haldane's rule has multiple genetic causes". Nature. 361 (6412): 532–533. Bibcode:1993Natur.361..532O. doi:10.1038/361532a0. PMID 8429905. S2CID 4304828.
^ ^a ^b 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. JSTOR 2462812. PMID 19425975. S2CID 35214550.
^ ^a ^b 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.x. PMID 14635874. S2CID 7127922.
^ 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. doi:10.1086/284701. JSTOR 2461884. S2CID 84357596.
^ ^a ^b Schilthuizen, M.; Giesbers, M. C.; Beukeboom, L. W. (2011). "Haldane's rule in the 21st century". Heredity. 107 (2): 95–102. doi:10.1038/hdy.2010.170. PMC 3178397. PMID 21224879.
^ 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. doi:10.1093/jhered/esr154. PMC 3331990. PMID 22378959.
^ 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. S2CID 25507884.
^ Koevoets, T.; Beukeboom, L. W. (2009). "Genetics of postzygotic isolation and Haldane's rule in haplodiploids". Heredity. 102 (1): 16–23. doi:10.1038/hdy.2008.44. PMID 18523445.
^ Sawamura, K. (1996). "Maternal effect as a cause of exceptions for Haldane's rule". Genetics. 143 (1): 609–611. doi:10.1093/genetics/143.1.609. PMC 1207293. PMID 8722809.
^ Ferree, Patrick M.; Barbash, Daniel A. (2009). "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.

v t e Biological rules
Rules	Allen's rule Shorter appendages in colder climates Bateson's rule Extra limbs mirror their neighbours Bergmann's rule Larger bodies in colder climates Cope's rule Bodies get larger over time Deep-sea gigantism Larger bodies in deep-sea animals Dollo's law Loss of complex traits is irreversible Eichler's rule Parasites co-vary with their hosts Emery's rule Insect social parasites are often in same genus as their hosts Fahrenholz's rule Host and parasite phylogenies become congruent Foster's rule (Insular gigantism, Insular dwarfism) Small species get larger, large species smaller, after colonizing islands Gause's law Complete competitors cannot coexist Gloger's rule Lighter coloration in colder, drier climates Haldane's rule Hybrid sexes that are absent, rare, or sterile, are heterogamic Harrison's rule Parasites co-vary in size with their hosts Hamilton's rule Genes increase in frequency when relatedness of recipient to actor times benefit to recipient exceeds reproductive cost to actor Kleiber's law An animals metabolic rate decreases with its size Hennig's progression rule In cladistics, the most primitive species are found in earliest, central, part of group's area Jarman–Bell principle The correlation between the size of an animal and its diet quality; larger animals can consume lower quality diet Jordan's rule Inverse relationship between water temperature and no. of fin rays, vertebrae Lack's principle Birds lay only as many eggs as they can provide food for Rapoport's rule Latitudinal range increases with latitude Rensch's rule Sexual size dimorphism increases with size when males are larger, decreases with size when females are larger Rosa's rule Groups evolve from character variation in primitive species to a fixed character state in advanced ones Schmalhausen's law A population at limit of tolerance in one aspect is vulnerable to small differences in any other aspect Thayer's law The top of an animals coloration is darker than the bottom Thorson's rule No. of eggs of benthic marine invertebrates decreases with latitude Van Valen's law Probability of extinction of a group is constant over time von Baer's laws Embryos start from a common form and develop into increasingly specialised forms Williston's law Parts in an organism become reduced in number and specialized in function
Related	Countergradient variation Where genetics opposes environment as a factor Gigantothermy Large ectothermic animals more easily maintain constant body temperature

v t e Speciation
Introduction History Laboratory experiments Glossary
Basic concepts	Species (Species complex) Reproductive isolation Anagenesis Cladogenesis Cospeciation Evidence of evolution
Geographic modes	Allopatric (Peripatric · Quantum · Centrifugal · Founder effect) Parapatric (Clines · Ring species) Sympatric
Isolating factors	Adaptation Natural selection Sexual selection Ecological speciation (Parallel speciation · Allochrony) Nonecological speciation Assortative mating Haldane's rule
Hybrid concepts	Hybrid speciation (Polyploidy · Klepton · Recombination) Reinforcement (evidence) Secondary contact Character displacement
Speciation in taxa	Birds Fish Insects Plants Fossils (Paleopolyploidy · Punctuated equilibrium · Macroevolution · Chronospecies)
Category Commons Evolutionary biology Portal WikiProject

Overview

Hypotheses

Exceptions

Notes

References

Further reading