Haldane's Rule Is Linked to Extraordinary Sex Ratios and Sperm Length in Stalk-Eyed Flies

By Wilkinson, Gerald S.; Christianson, Sarah J. et al. | Genetics, November 2014 | Go to article overview

Haldane's Rule Is Linked to Extraordinary Sex Ratios and Sperm Length in Stalk-Eyed Flies


Wilkinson, Gerald S., Christianson, Sarah J., Brand, Cara L., Ru, George, Shell, Wyatt, Genetics


A major challenge to those who study spéciation is to determine the causes of early reproductive isolation between incipient species. One avenue for gaining insight into this issue is to investigate the causes of Haldane's rule, i.e., the observation that the heterogametic sex of hybrid offspring are more likely to be sterile or inviable than the homogametic sex (Haldane 1922). This phenomenon has been observed in a wide range of animal taxa and is believed to be a nearly ubiquitous phase of early spéciation (Orr 1997). Given that alleles for sterility or inviability are expected to be selected against within populations, models for the evolution of hybrid dysfunction typically assume two or more genes, each of which is neutral or advantageous within a population but have deleterious joint effects when mis-Copyright matched between populations. Two nonmutually exclusive explanations (Turelli 1998) have been proposed for why these epistatic interactions, known as Dobzhansky-Muller incompatibilities (Dobzhansky 1937; Muller 1940, 1942; Orr 1995), should arise more quickly in the heterogametic sex.

The dominance hypothesis (Muller 1942; Orr 1993; Turelli and Orr 1995) assumes that if genes causing hybrid dysfunction are recessive, then the heterogametic sex will be affected more than the homogametic sex. This result is expected because the degenerate (or missing, in XO taxa) sex chromosome possessed by the heterogametic sex fails to mask recessive alleles present on its homolog. This hypothesis potentially applies to all taxa with a degenerate sex chromosome, whether male or female heterogametic. The faster-male hypothesis (Wu and Davis 1993; Wu et αi. 1996) states that male-specific sterility factors accumulate faster than female-specific factors, because sexual selection causes more rapid change in loci with male-specific reproductive function. This hypothesis applies to male-heterogametic taxa or taxa where the chromosome that determines maleness is not degenerate (as in Aedes mosquitoes, Presgraves and Orr 1998).

In 1991 two publications independently proposed a third hypothesis to explain incompatibilities in heterogametic hybrids: divergence of sex chromosome meiotic drive sys- tems (Frank 1991; Hurst and Pomiankowski 1991). Sex chromosome meiotic drive refers to non-Mendelian passage of the X (or Y) chromosome into gametes and causes biased progeny sex ratios. Drive is expected to be more common on sex chromosomes than autosomes because the nonrecombin- ing portions of the X and Y each act as a cooperative unit with regard to biased transmission (Dawkins 1982). Conse- quently, two-locus drive systems that require linkage be- tween target and responder loci to prevent self-destruction can more easily evolve on the sex chromosomes (Hurst and Pomiankowski 1991). Because population sex-ratio bias gen- erates strong selection to restore sex-ratio equality, suppres- sors elsewhere in the genome are expected to evolve rapidly (Leigh 1971; Hartl 1975). Thus, the drive hypothesis assumes that hybrid incompatibilities arise as a result of co- evolution between drive and modifiers of drive that alter- nately suppress and enhance it within populations over time.

Unlike the faster-male theory, the drive hypothesis can apply to either male- or female-heterogametic taxa (Tao and Hartl 2003) because there are two different mechanisms for producing meiotic drive. In one type, loci attack their coun- terparts on homologous chromosomes in male gametes and kill the sperm in which they are carried, which could lead to Haldane's rule in male-heterogametic species. In the other type, centromeres compete to reach the ovum during meio- sis in females instead of being relegated to a polar body (Novitski 1951; Henikoff and Malik 2002). Covariation in satellite sequence between the centromere and centromeric histones is consistent with an arms race to ensure successful spindle attachment (Malik and Henikoff 2001; Malik et al. 2002) and differences in centromeric and telomeric sequences between populations can disrupt meiosis in hybrid males and cause sterility (McKee et al. …

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