Haldane's Rule - Hypotheses

Hypotheses

Many different hypotheses have been advanced to address the genetic basis for hybrid inferiority in the heterogametic sex. 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. In contrast to these views that emphasize genetic mechanisms, another view hypothesizes that population dynamics during population divergence may cause Haldane’s rule. The following are the main genetic hypotheses.

• Dominance: Homogametic hybrids are only affected by deleterious sex-linked alleles involved in breeding incompatibilities if those alleles are dominant, because they carry another allele that can compensate for recessive mutations. However, heterogametic hybrids, which carry only a single copy of a given sex-linked gene, will be affected by mutations regardless of dominance. Thus, sex-linked incompatibility between diverging populations is more likely to be displayed in the heterogametic sex than homogametic sex. Similarly, the effects of negative X-linked alleles in humans are visible more often in men than women, such as color blindness or haemophilia.
• The "faster male": Male genes are thought to evolve faster due to sexual selection. 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 sex chromosomes may evolve more quickly than autosomal genes, causing a larger effect in reproductive isolation.
• 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.

Data from multiple phylogenetic groups support a combination of dominance and faster X-chromosome theories.

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.

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.