Reproductive isolation in the Elegans-Group of Caenorhabditis

Baird, Scott Everet; Seibert, Sara Rose

doi:10.4236/ns.2013.54a004

Cited by 14 publications

(23 citation statements)

References 64 publications

(129 reference statements)

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“…We rule out a major influence of temporal pleiotropy masking the existence of late‐acting inviability, assuming independence of penetrance in different developmental stages, because F1 individuals that manage to survive past L1 also are almost certain to survive to adulthood, despite being genetically identical to F1 animals that die as embryos. Embryonic arrest is seen in many other Caenorhabditis interspecific crosses (Baird and Yen ; Baird and Seibert ; Dey et al. ), suggesting embryogenesis could be particularly sensitive to disruption in Caenorhabditis and, along with hybrid male sterility (Dey et al.…”

Section: Discussionmentioning

confidence: 99%

“…; Dey et al. ; Baird and Seibert ). In particular, crosses between C. briggsae and C. nigoni exhibit Haldane's rule, producing some viable and fertile XX hybrid females, and a small number of sterile hybrid XØ males (Woodruff et al.…”

mentioning

confidence: 98%

“…Caenorhabditis nematodes provide a classic genetic model organism in biology, but only the recent discovery of close sister species pairs has empowered this system for studies of the genetics and evolution of reproductive isolation (Woodruff et al 2010;Dey et al 2012;Baird and Seibert 2013). In particular, crosses between C. briggsae and C. nigoni exhibit Haldane's rule, producing some viable and fertile XX hybrid females, and a small number of sterile hybrid XØ males (Woodruff et al 2010;Kozlowska et al 2012).…”

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confidence: 99%

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Gametic selection, developmental trajectories, and extrinsic heterogeneity in Haldane's rule

2015

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Deciphering the genetic and developmental causes of the disproportionate rarity, inviability, and sterility of hybrid males, Haldane's rule, is important for understanding the evolution of reproductive isolation between species. Moreover, extrinsic and prezygotic factors can contribute to the magnitude of intrinsic isolation experienced between species with partial reproductive compatibility. Here, we use the nematodes Caenorhabditis briggsae and C. nigoni to quantify the sensitivity of hybrid male viability to extrinsic temperature and developmental timing, and test for a role of mito-nuclear incompatibility as a genetic cause. We demonstrate that hybrid male inviability manifests almost entirely as embryonic, not larval, arrest and is maximal at the lowest rearing temperatures, indicating an intrinsic-by-extrinsic interaction to hybrid inviability. Crosses using mitochondrial substitution strains that have reciprocally introgressed mitochondrial and nuclear genomes show that mito-nuclear incompatibility is not a dominant contributor to postzygotic isolation and does not drive Haldane's rule in this system. Crosses also reveal that competitive superiority of X-bearing sperm provides a novel means by which postmating prezygotic factors exacerbate the rarity of hybrid males. These findings highlight the important roles of gametic, developmental, and extrinsic factors in modulating the manifestation of Haldane's rule.

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Section: Discussionmentioning

confidence: 99%

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confidence: 98%

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confidence: 99%

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Gametic selection, developmental trajectories, and extrinsic heterogeneity in Haldane's rule

2015

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“…If only a few DMIs of large effect are responsible for reproductive isolation, however, then cross asymmetry also could result simply from stochasticity between lineages in the origin and dominance of DMI effects, irrespective of sex linkage. Striking asymmetry occurs in reciprocal crosses both for closely related species of Caenorhabditis (capable of forming viable and fertile hybrids; Dey et al., ; Dey et al., ; Kozlowska et al., ; Woodruff et al., ) and distantly related species (rare viable and completely sterile hybrids; Baird & Seibert, ; Baird & Yen, ) (Table ). The conspicuous influence of the X‐chromosome in interspecies hybrid dysfunction makes the X‐chromosome an obvious candidate for contributing to such asymmetry, which is consistent with data for both C. briggsae‐nigoni hybrids and C. remanei‐latens hybrids (Bundus et al., , ).…”

Section: Darwin's Corollary To Haldane's Rulementioning

confidence: 99%

X exceptionalism in Caenorhabditis speciation

Cutter

2017

Molecular Ecology

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Speciation genetics research in diverse organisms shows the X-chromosome to be exceptional in how it contributes to "rules" of speciation. Until recently, however, the nematode phylum has been nearly silent on this issue, despite the model organism Caenorhabditis elegans having touched most other topics in biology. Studies of speciation with Caenorhabditis accelerated with the recent discovery of species pairs showing partial interfertility. The resulting genetic analyses of reproductive isolation in nematodes demonstrate key roles for the X-chromosome in hybrid male sterility and inviability, opening up new understanding of the genetic causes of Haldane's rule, Darwin's corollary to Haldane's rule, and enabling tests of the large-X effect hypothesis. Studies to date implicate improper chromatin regulation of the X-chromosome by small RNA pathways as integral to hybrid male dysfunction. Sexual transitions in reproductive mode to self-fertilizing hermaphroditism inject distinctive molecular evolutionary features into the speciation process for some species. Caenorhabditis also provides unique opportunities for analysis in a system with XO sex determination that lacks a Y-chromosome, sex chromosome-dependent sperm competition differences and mechanisms of gametic isolation, exceptional accessibility to the development process and rapid experimental evolution. As genetic analysis of reproductive isolation matures with investigation of multiple pairs of Caenorhabditis species and new species discovery, nematodes will provide a powerful complement to more established study organisms for deciphering the genetic basis of and rules to speciation.

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“…The genetic underpinnings to hybrid incompatibility have been studied most extensively in genetic model organisms, most notably Drosophila (Presgraves , ; Maheshwari and Barbash ). However, Caenorhabditis nematodes largely have been a dormant player in speciation research, despite the breadth of their application to other topics in developmental biology and evolution (Cutter et al ; Baird and Seibert ). Historically, high interspecies divergence for a paucity of species known to science, coupled with no species pairs capable of yielding fertile hybrid progeny, has hampered genetic analysis of species barriers in this group.…”

Section: Introductionmentioning

confidence: 99%

Gonad morphogenesis defects drive hybrid male sterility in asymmetric hybrid breakdown of Caenorhabditis nematodes

Dey

Jin

Chen

et al. 2014

Evolution and Development

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Determining the causes and evolution of reproductive barriers to gene flow between populations, speciation, is the key to understanding the origin of diversity in nature. Many species manifest hybrid breakdown when they intercross, characterized by increasingly exacerbated problems in later generations of hybrids. Recently, Caenorhabditis nematodes have emerged as a genetic model for studying speciation, and here we investigate the nature and causes of hybrid breakdown between C. remanei and C. latens. We quantify partial F1 hybrid inviability and extensive F2 hybrid inviability; the ~75% F2 embryonic arrest occurs primarily during gastrulation or embryonic elongation. Moreover, F1 hybrid males exhibit Haldane’s rule asymmetrically for both sterility and inviability, being strongest when C. remanei serves as maternal parent. We show that the mechanism by which sterile hybrid males are incapable of transferring sperm or a copulatory plug involves defective gonad morphogenesis, which we hypothesize results from linker cell defects in migration and/or cell death during development. This first documented case of partial hybrid male sterility in Caenorhabditis follows expectations of Darwin’s corollary to Haldane’s rule for asymmetric male fitness, providing a powerful foundation for molecular dissection of intrinsic reproductive barriers and divergence of genetic pathways controlling organ morphogenesis.

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Reproductive isolation in the Elegans-Group of Caenorhabditis

Cited by 14 publications

References 64 publications

Gametic selection, developmental trajectories, and extrinsic heterogeneity in Haldane's rule

Gametic selection, developmental trajectories, and extrinsic heterogeneity in Haldane's rule

X exceptionalism in Caenorhabditis speciation

Gonad morphogenesis defects drive hybrid male sterility in asymmetric hybrid breakdown of Caenorhabditis nematodes

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