Haldane's rule
Encyclopedia
Haldane's rule or Haldane's law was formulated in 1922 by the British evolutionary biologist J.B.S. Haldane. It describes hybrid sterility in species and is extended to describe speciation
in evolutionary theory
, in two parts: the rule of hybrid sterility and the rule of hybrid inviability
. According to the rule of hybrid sterility, when the resulting offspring of parents crossed from different lineages
exhibits sterility but is otherwise healthy, that offspring will tend to be of the heterogametic sex, which exhibits two different sex chromosomes (as in XY). Heterogametes are also typically subject to greater morphological deformities than homogametic hybrids. Haldane's accompanying rule for hybrid inviability states that when two parental lineages become so evolutionarily divergent
as to exhibit genetic differences, but do not become mechanically isolated
, fusion of the gametes
may be uncooperative, causing inviability and the preferential production of the homogametic sex, which exhibits two of the same sex chromosomes (as in XX). The heterogametic sex is rare in this case.
This pattern holds true in both organisms in which males are the heterogametic sex (as in Drosophila and mammals, including humans) as well as in organisms where the reverse is true, females being heterogametic (as in birds).
According to the rule, the first stage of speciation occurs when all offspring produced by two differing lineages are hybrids, although viable. As genetic divergence continues, incompatibilities preventing the fusion of gametes, the development of the embryo
, or the development of the offspring to adult maturity
arise, causing hybrid inviability. The development of prezygotic barriers to reproduction ensues at this stage, in the form of anatomical, temporal, or behavioral incompatibility. By definition, the two lineages may be referred to as different species
, as they may no longer interbreed naturally.
, or even why only homogametic offspring are almost always produced in hybridization. A variety of factors have been hypothesized to contribute to these phenomena.
Data from multiple phylogenetic groups support a "dominance and faster X–chromosome" theory .
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 elephant
s, suggesting a faster evolution of male traits.
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.
, where it is proposed to function through maternal effect
genes, and their interaction with species specific heterochromatin
.
Speciation
Speciation is the evolutionary process by which new biological species arise. The biologist Orator F. Cook seems to have been the first to coin the term 'speciation' for the splitting of lineages or 'cladogenesis,' as opposed to 'anagenesis' or 'phyletic evolution' occurring within lineages...
in evolutionary theory
Evolution
Evolution is any change across successive generations in the heritable characteristics of biological populations. Evolutionary processes give rise to diversity at every level of biological organisation, including species, individual organisms and molecules such as DNA and proteins.Life on Earth...
, in two parts: the rule of hybrid sterility and the rule of hybrid inviability
Hybrid inviability
Hybrid inviability is a post-zygotic barrier, which reduces a hybrid's capacity to mature into a healthy, fit adult. The relatively low health of these hybrids relative to pure-breed individuals prevents gene flow between species...
. According to the rule of hybrid sterility, when the resulting offspring of parents crossed from different lineages
Lineage
Lineage may refer to:- Science :* Lineage or kinship, descent group that can demonstrate their common descent from an apical ancestor or a direct line of decent from an ancestor....
exhibits sterility but is otherwise healthy, that offspring will tend to be of the heterogametic sex, which exhibits two different sex chromosomes (as in XY). Heterogametes are also typically subject to greater morphological deformities than homogametic hybrids. Haldane's accompanying rule for hybrid inviability states that when two parental lineages become so evolutionarily divergent
Genetic divergence
Genetic divergence is the process in which two or more populations of an ancestral species accumulate independent genetic changes through time, often after the populations have become reproductively isolated for some period of time...
as to exhibit genetic differences, but do not become mechanically isolated
Reproductive isolation
The mechanisms of reproductive isolation or hybridization barriers are a collection of mechanisms, behaviors and physiological processes that prevent the members of two different species that cross or mate from producing offspring, or which ensure that any offspring that may be produced is not...
, fusion of the gametes
Gamete
A gamete is a cell that fuses with another cell during fertilization in organisms that reproduce sexually...
may be uncooperative, causing inviability and the preferential production of the homogametic sex, which exhibits two of the same sex chromosomes (as in XX). The heterogametic sex is rare in this case.
This pattern holds true in both organisms in which males are the heterogametic sex (as in Drosophila and mammals, including humans) as well as in organisms where the reverse is true, females being heterogametic (as in birds).
According to the rule, the first stage of speciation occurs when all offspring produced by two differing lineages are hybrids, although viable. As genetic divergence continues, incompatibilities preventing the fusion of gametes, the development of the embryo
Embryo
An embryo is a multicellular diploid eukaryote in its earliest stage of development, from the time of first cell division until birth, hatching, or germination...
, or the development of the offspring to adult maturity
Maturity
Maturity may refer to:*Sexual maturity, the stage when an organism can reproduce, though it is distinct from adulthood*Mature technology, a term indicating that a technology has been in use and development for long enough that most of its initial problems have been overcome*Maturity , a geological...
arise, causing hybrid inviability. The development of prezygotic barriers to reproduction ensues at this stage, in the form of anatomical, temporal, or behavioral incompatibility. By definition, the two lineages may be referred to as different species
Species
In biology, a species is one of the basic units of biological classification and a taxonomic rank. A species is often defined as a group of organisms capable of interbreeding and producing fertile offspring. While in many cases this definition is adequate, more precise or differing measures are...
, as they may no longer interbreed naturally.
Further explanation of phenomena
Although Haldane's rule may prove to be one of "the strongest patterns in evolutionary biology," a sufficient explanation of the occurrence of hybrid sterility and hybrid inviability has only been theorized. It is unclear as to why hybrids of the heterogametic sex are much more greatly afflicted by deformitiesSex chromosome disorders
Sex chromosome disorders belong to a group of genetic conditions that are caused or affected by the loss or damage of sex chromosomes.It may refer to:* 47,XXX* 48, XXXX* 49 XXXXY syndrome* 49, XXXXX* Klinefelter's syndrome* Turner syndrome...
, or even why only homogametic offspring are almost always produced in hybridization. A variety of factors have been hypothesized to contribute to these phenomena.
- The maternal dominance hypothesis suggests that 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.
- Faster male hypothesis: Male genes evolve faster due to sexual selection.
- 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 .
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 elephant
Asian Elephant
The Asian or Asiatic elephant is the only living species of the genus Elephas and distributed in Southeast Asia from India in the west to Borneo in the east. Three subspecies are recognized — Elephas maximus maximus from Sri Lanka, the Indian elephant or E. m. indicus from mainland Asia, and E. m....
s, suggesting a faster evolution of male traits.
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
Color blindness
Color blindness or color vision deficiency is the inability or decreased ability to see color, or perceive color differences, under lighting conditions when color vision is not normally impaired...
or haemophilia
Haemophilia
Haemophilia is a group of hereditary genetic disorders that impair the body's ability to control blood clotting or coagulation, which is used to stop bleeding when a blood vessel is broken. Haemophilia A is the most common form of the disorder, present in about 1 in 5,000–10,000 male births...
.
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.
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 DrosophilaDrosophila
Drosophila is a genus of small flies, belonging to the family Drosophilidae, whose members are often called "fruit flies" or more appropriately pomace flies, vinegar flies, or wine flies, a reference to the characteristic of many species to linger around overripe or rotting fruit...
, where it is proposed to function through maternal effect
Maternal effect
A maternal effect is a situation where the phenotype of an organism is determined not only by the environment it experiences and its genotype, but also by the environment and phenotype of its mother...
genes, and their interaction with species specific heterochromatin
Heterochromatin
Heterochromatin is a tightly packed form of DNA, which comes in different varieties. These varieties lie on a continuum between the two extremes of constitutive and facultative heterochromatin...
.
Other references
- Coyne, J.A. (1985): The genetic basis of Haldane's rule. NatureNatureNature, in the broadest sense, is equivalent to the natural world, physical world, or material world. "Nature" refers to the phenomena of the physical world, and also to life in general...
314(6013): :736–738. Retrieved 2007-JAN-26. NCBI PubmedNational Center for Biotechnology InformationThe National Center for Biotechnology Information is part of the United States National Library of Medicine , a branch of the National Institutes of Health. The NCBI is located in Bethesda, Maryland and was founded in 1988 through legislation sponsored by Senator Claude Pepper...
Abstract. - Forsdyke, Donald (2005): Haldane's rule. Version of 2005-DEC-6. Retrieved 2006-OCT-11.