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

Abstract

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.

X exceptionalism in Caenorhabditis speciation

“…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., , ). To date, however, analysis of introgression lines between species is limited to just a single species pair and in just one direction of introgression ( C. briggsae DNA introgressed in to C. nigoni ) (Bi et al., ).…”

“…In addition to genetically intrinsic contributions of incompatibilities to Haldane's rule in Caenorhabditis , extrinsic and developmental factors also modulate the magnitude of hybrid male inviability. Specifically, hybrid male inviability and therefore Haldane's rule are disproportionately strong at low rearing temperatures for C. briggsae‐nigoni hybrids (Bundus, Alaei, & Cutter, ). Moreover, not all developmental stages equally contribute to hybrid inviability.…”

“…No driving X elements are known from Caenorhabditis through mechanisms similar to those described for Drosophila (McDermott & Noor, ; Phadnis & Orr, ; Tao, Hartl, & Laurie, ). At the postmating prezygotic level, however, greater sperm competitiveness of X‐bearing sperm in C. briggsae mimics a drive‐like process and leads to skewed sex ratios in both conspecific and heterospecific crosses (Bundus et al., ; LaMunyon & Ward, ). While this phenomenon influences the manifestation of Haldane's rule (Bundus et al., ), the genetic cause remains unknown and so it is unclear whether it has the potential to contribute to a large‐X effect at the postzygotic level.…”

Rapid genome shrinkage in a self-fertile nematode reveals sperm competition proteins

“…They remain partially interfertile, yet have numerous genetic and reproductive incompatibilities (9, 15, 17–19). To compare their genomes , we assembled the C. nigoni genome from 20-kb Pacific Biosciences (PacBio) and Illumina short-read libraries (table S1; (20)).…”

Convergent evolution of sperm gigantism and the developmental origins of sperm size variability inCaenorhabditisnematodes

“…In C. briggsae , and perhaps other species, sperm bearing the X chromosome enjoy a fertilization advantage over nullo‐X sperm (LaMunyon and Ward ; Bundus et al. ). Differential sperm sizes owing to asymmetric meiotic cell division provides one possible mechanism for manifesting such an advantage, as occurs in a species of Rhabditis nematodes (Shakes et al.…”