Hybridization and Postzygotic Isolation Patterns in Pigeons and Doves

Lijtmaer, Darío A; Mahler, Bettina; Tubaro, Pablo L.

doi:10.1554/02-656

Cited by 48 publications

(53 citation statements)

References 36 publications

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“…Sub-populations in a metapopulation with such selective, uneven gene flow could enjoy a relative independence for the benefit of local adaptation and, at the same time, share advantageous mutations through limited gene flow. This notion is in agreement with the high genetic similarity between many distinct species that are not separated by strong physical barriers, such as those observed in Drosophila (Ranz et al, 2003), birds (Crochet et al, 2003;Lijtmaer et al, 2003) and Lepidoptera (Presgraves, 2002). Given the prevalence of Haldane's rule, sex-biased genetic incompatibilities could be a major driving force behind such genomic divergence.…”

Section: Discussionsupporting

confidence: 80%

Differential barrier strength and allele frequencies in hybrid zones maintained by sex-biased hybrid incompatibilities

2007

Heredity

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In animals, hybrid sterility and inviability between closely related species often affect only the heterogametic sex (XY). This widespread phenomenon, known as Haldane's rule, is an early speciation event found across broad taxa, but the role of heterogametic hybrid incompatibilities, as opposed to homogametic ones, as a barrier in a speciation process remains obscure. It has been hypothesized that heterogametic incompatibility may be a more efficient mechanism in driving speciation. The population dynamics after (rather than before) the occurrence of sex-biased incompatibilities may account for Haldane's rule. In this study, a recursion model of hybrid zones was developed to investigate the differences between heterogametic and homogametic incompatibilities. The selection strengths and selection patterns of sex chromosome-linked, two-locus BatesonDobzhansky-Muller (BDM) genetic incompatibilities were examined. It is noted that a sex-biased hybrid incompatibility in a hybrid zone confers asymmetric and uneven impedance to gene flow. The clines of different loci in such a hybrid zone displayed diverse differentiation in their width, steepness and asymmetry. Alleles involved in the incompatibility face much stronger resistance to cross a hybrid zone. Different sexbiased BDM incompatibilities also affect the flow of neutral alleles differently. Compared to a homogametic one, heterogametic incompatibility is a weaker but more asymmetric barrier. These unique patterns of gene flow may explain uneven divergence among different genomic regions during speciation between some closely related species.

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Section: Discussionsupporting

confidence: 80%

Differential barrier strength and allele frequencies in hybrid zones maintained by sex-biased hybrid incompatibilities

2007

Heredity

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“…Because S is expected to increase roughly quadratically (Orr 1995;Orr and Turelli 2001) as two-locus DMIs accumulate (and even faster for multilocus DMIs), a ¼ 0.5 would produce a roughly linear decline of hybrid fitness with divergence time, whereas a ¼ 1 and a ¼ 1.5 would produce a roughly quadratic or cubic decline, respectively. Given that metaanalyses reveal at most a slightly faster than linear decline of hybrid fitness with divergence (e.g., Lijtmaer et al 2003;Bolnick and Near 2005), we focus our numerical examples on an intermediate case, a ¼ 0.75.…”

Section: Models and Analysesmentioning

confidence: 99%

Asymmetric Postmating Isolation: Darwin's Corollary to Haldane's Rule

2007

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Asymmetric postmating isolation, where reciprocal interspecific crosses produce different levels of fertilization success or hybrid sterility/inviability, is very common. Darwin emphasized its pervasiveness in plants, but it occurs in all taxa assayed. This asymmetry often results from Dobzhansky-Muller incompatibilities (DMIs) involving uniparentally inherited genetic factors (e.g., gametophyte-sporophyte interactions in plants or cytoplasmic-nuclear interactions). Typically, unidirectional (U) DMIs act simultaneously with bidirectional (B) DMIs between autosomal loci that affect reciprocal crosses equally. We model both classes of two-locus DMIs to make quantitative and qualitative predictions concerning patterns of isolation asymmetry in parental species crosses and in the hybrid F 1 generation. First, we find conditions that produce expected differences. Second, we present a stochastic analysis of DMI accumulation to predict probable levels of asymmetry as divergence time increases. We find that systematic interspecific differences in relative rates of evolution for autosomal vs. nonautosomal loci can lead to different expected F 1 fitnesses from reciprocal crosses, but asymmetries are more simply explained by stochastic differences in the accumulation of U DMIs. The magnitude of asymmetry depends primarily on the cumulative effects of U vs. B DMIs (which depend on heterozygous effects of DMIs), the average number of DMIs required to produce complete reproductive isolation (more asymmetry occurs when fewer DMIs are required), and the shape of the function describing how fitness declines as DMIs accumulate. Comparing our predictions to data from diverse taxa indicates that unidirectional DMIs, specifically involving sex chromosomes, cytoplasmic elements, and maternal effects, are likely to play an important role in postmating isolation.The degree of sterility does not strictly follow systematic affinity, but is governed by several curious and complex laws. It is generally different, and sometimes wildly different, in reciprocal crosses between the same two species. Darwin (1859)

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“…Laurie (1997) provided a list of all taxa examined thus far. More recent authors have focused in more detail on taxa with female heterogamety, viz Aves (Price and Bouvier, 2002;Tubaro and Lijtmaer, 2002;Lijtmaer et al, 2003), Lepidoptera (Presgraves, 2002) and certain Teleostei (Russell, 2003). The most recent update is by Coyne and Orr (2004) who provide a summary table of the number of species that support HR.…”

Section: Aimsmentioning

confidence: 99%

Haldane's rule in the 21st century

2011

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Haldane's Rule (HR), which states that 'when in the offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous (heterogametic) sex', is one of the most general patterns in speciation biology. We review the literature of the past 15 years and find that among the B85 new studies, many consider taxa that traditionally have not been the focus for HR investigations. The new studies increased to nine, the number of 'phylogenetically independent' groups that comply with HR. They continue to support the dominance and faster-male theories as explanations for HR, although due to increased reliance on indirect data (from, for example, differential introgression of cytoplasmic versus chromosomal loci in natural hybrid zones) unambiguous novel results are rare. We further highlight how research on organisms with sex determination systems different from those traditionally considered may lead to more insight in the underlying causes of HR. In particular, haplodiploid organisms provide opportunities for testing specific predictions of the dominance and faster X chromosome theory, and we present new data that show that the faster-male component of HR is supported in hermaphrodites, suggesting that genes involved in male function may evolve faster than those expressed in the female function.

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Hybridization and Postzygotic Isolation Patterns in Pigeons and Doves

Cited by 48 publications

References 36 publications

Differential barrier strength and allele frequencies in hybrid zones maintained by sex-biased hybrid incompatibilities

Differential barrier strength and allele frequencies in hybrid zones maintained by sex-biased hybrid incompatibilities

Asymmetric Postmating Isolation: Darwin's Corollary to Haldane's Rule

Haldane's rule in the 21st century

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