Patterns of Reproductive Isolation in Toads

Malone, John H.; Fontenot, Brian E.

doi:10.1371/journal.pone.0003900

Cited by 100 publications

(127 citation statements)

References 74 publications

(108 reference statements)

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“…The evolution of new, reproductively isolated species usually involves the gradual accumulation of multiple prezygotic and postzygotic reproductive isolating barriers over time Orr, 1989, 1997;Moyle et al, 2004;Malone and Fontenot, 2008;Scopece et al, 2008). An exception to this is hybrid speciation, where reproductive isolation can evolve quite quickly (James and Abbott, 2005;Mallett, 2007;Buerkle and Rieseberg, 2008).…”

Section: Introductionmentioning

confidence: 99%

Genomic collinearity and the genetic architecture of floral differences between the homoploid hybrid species Iris nelsonii and one of its progenitors, Iris hexagona

Taylor

Rojas

et al. 2012

Heredity

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Hybrid speciation represents a relatively rapid form of diversification. Early models of homoploid hybrid speciation suggested that reproductive isolation between the hybrid species and progenitors primarily resulted from karyotypic differences between the species. However, genic incompatibilities and ecological divergence may also be responsible for isolation. Iris nelsonii is an example of a homoploid hybrid species that is likely isolated from its progenitors primarily by strong prezygotic isolation, including habitat divergence, floral isolation and post-pollination prezygotic barriers. Here, we used linkage mapping and quantitative trait locus (QTL) mapping approaches to investigate genomic collinearity and the genetic architecture of floral differences between I. nelsonii and one of its progenitor species I. hexagona. The linkage map produced from this cross is highly collinear with another linkage map produced between I. fulva and I. brevicaulis (the two other species shown to have contributed to the genomic makeup of I. nelsonii), suggesting that karyotypic differences do not contribute substantially to isolation in this homoploid hybrid species. Similar to other studies of the genetic architecture of floral characteristics, at least one QTL was found that explained 420% variance in each color trait, while minor QTLs were detected for each morphological trait. These QTLs will serve as hypotheses for regions under selection by pollinators.

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Section: Introductionmentioning

confidence: 99%

Genomic collinearity and the genetic architecture of floral differences between the homoploid hybrid species Iris nelsonii and one of its progenitors, Iris hexagona

Taylor

Rojas

et al. 2012

Heredity

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“…Empirical support for turnovers has been gathered from several fish [e.g. Tanaka et al, 2007;Cnaani et al, 2008;Ross et al, 2009] and amphibian systems, including Ranidae [Hotz et al, 1997;Miura, 2007] and Bufonidae [Malone and Fontenot, 2008;Stöck et al, 2011aStöck et al, , 2013.…”

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Maintenance of Ancestral Sex Chromosomes in Palearctic Tree Frogs: Direct Evidence from <b><i>Hyla orientalis</i></b>

Stöck

Savary²,

Zaborowska³

et al. 2013

Sex Dev

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Contrasting with the situation found in birds and mammals, sex chromosomes are generally homomorphic in poikilothermic vertebrates. This homomorphy was recently shown to result from occasional X-Y recombinations (not from turnovers) in several European species of tree frogs (Hyla arborea, H. intermedia and H. molleri). Because of recombination, however, alleles at sex-linked loci were rarely diagnostic at the population level; support for sex linkage had to rely on multilocus associations, combined with occasional sex differences in allelic frequencies. Here, we use direct evidence, obtained from anatomical and histological analyses of offspring with known pedigrees, to show that the Eastern tree frog (H. orientalis) shares the same pair of sex chromosomes, with identical patterns of male heterogamety and complete absence of X-Y recombination in males. Conservation of an ancestral pair of sex chromosomes, regularly rejuvenated via occasional X-Y recombination, seems thus a widespread pattern among Hyla species. Sibship analyses also identified discrepancies between genotypic and phenotypic sex among offspring, associated with abnormal gonadal development, suggesting a role for sexually antagonistic genes on the sex chromosomes.

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“…This observation is consistent with the deterministic asymmetry hypothesis, but was somewhat surprising in light of the relatively small effect expected with plausible parameters for mitonuclear contributions to hybrid inviability. Here we examine whether this deterministic pattern holds using more extensive data from another clade, toads of the genus Bufo (taxonomy following Pauly et al 2009, which maintains consistency with the names used in Malone and Fontenot 2008). We describe patterns of asymmetry produced at different stages of F 1 formation and development and at different levels of phylogenetic divergence.…”

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confidence: 98%

“…Here we examine whether this deterministic pattern holds using more extensive data from another clade, toads of the genus Bufo (taxonomy following Pauly et al 2009, which maintains consistency with the names used in Malone and Fontenot 2008). We describe patterns of asymmetry produced at different stages of F 1 formation and development and at different levels of phylogenetic divergence.We examine the success of Blair's (1972) experimental crosses as summarized by Malone and Fontenot (2008) across three stages of toad development: fertilization, hatching, and metamorphosis. These stages differ in whether mitonuclear incompatibilities can plausibly explain observed asymmetries:…”

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Explaining Darwin’s Corollary to Haldane’s Rule: The Role of Mitonuclear Interactions in Asymmetric Postzygotic Isolation Among Toads

et al. 2014

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We examine the basis of Darwin's corollary to Haldane's rule, which describes viability and fertility differences between F 1 produced from reciprocal crosses. We analyzed asymmetries in hybrid viability from .100 reciprocal crosses involving 36 toad species to test whether relatively high rates of mitochondrial vs. nuclear evolution produce dams with systematically less viable F 1 hybrid progeny. We find no such effect, suggesting a predominant role for stochastic accumulation of asymmetric epistatic incompatibilities.A S Darwin (1859, Chap. 8) noted, interspecific reciprocal crosses often differ in whether fertilization occurs and in the viability and fecundity of F 1 hybrids. Even under optimal laboratory conditions, reciprocal F 1 s often show viability or fecundity differences. This pattern of asymmetric intrinsic postzygotic isolation has been dubbed "Darwin's corollary to Haldane's rule" (Turelli and Moyle 2007). While asymmetric fertilization success can be produced under autosomal genetic control, Darwin's corollary requires deleterious epistatic interactions (i.e., Dobzhansky-Muller incompatibilities, DMIs) involving uniparentally inherited factors such as mitochondria, sex chromosomes, epigenetic programming, or maternal effects (Turelli and Moyle 2007), because only uniparentally inherited factors will differentially affect F 1 produced from reciprocal crosses.Turelli and Moyle (2007) contrasted deterministic vs. stochastic explanations for Darwin's corollary, depending on whether the cross that produces less fit hybrids is predictable from relative rates of evolution for uniparentally vs. biparentally inherited factors. Differences in the relative rates of evolution can lead to different expected fitnesses from reciprocal crosses. Consider the species pair A-B. If the proportion of mitochondrial to nuclear substitutions in lineage A exceeds that in lineage B, we expect more mitonuclear DMIs in AB F 1 hybrids with A mothers vs. BA hybrids with B mothers, simply because there are more potential incompatibilities in the AB cross than in the BA cross. Thus, if mitonuclear DMIs contribute significantly to lowered interpopulation (Burton et al. 2006;Ellison and Burton 2008;Montooth et al. 2010; Meiklejohn et al. 2013) or interspecific (e.g., Fishman andWillis 2006;Lee et al. 2008; Rieseberg and Blackman 2010) fitness, as often argued (e.g., Rand et al. 2004;Gershoni et al. 2009;Lane 2011;Burton and Barreto 2012), directional asymmetry may be predictable from relative rates of mitochondrial vs. nuclear evolution. Turelli and Moyle (2007) conjectured that the deterministic signal associated with directional effects produced by a particular class of DMIs (e.g., mitonuclear incompatibilities) was likely to be overwhelmed by both stochastic effects and other classes of asymmetric incompatibilities. The theoretical analyses pioneered by Orr (1993) describe the accumulation of DMIs as rare--independent and inherently stochastic--events associated with molecular differences between diverging taxa. Diff...

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Patterns of Reproductive Isolation in Toads

Cited by 100 publications

References 74 publications

Genomic collinearity and the genetic architecture of floral differences between the homoploid hybrid species Iris nelsonii and one of its progenitors, Iris hexagona

Genomic collinearity and the genetic architecture of floral differences between the homoploid hybrid species Iris nelsonii and one of its progenitors, Iris hexagona

Maintenance of Ancestral Sex Chromosomes in Palearctic Tree Frogs: Direct Evidence from <b><i>Hyla orientalis</i></b>

Explaining Darwin’s Corollary to Haldane’s Rule: The Role of Mitonuclear Interactions in Asymmetric Postzygotic Isolation Among Toads

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