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

Abstract

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.

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

“…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. ), might be among the earliest intrinsic postzygotic barriers to arise during speciation in these organisms.…”

“…), suggesting embryogenesis could be particularly sensitive to disruption in Caenorhabditis and, along with hybrid male sterility (Dey et al. ), might be among the earliest intrinsic postzygotic barriers to arise during speciation in these organisms. If cell division is a crucial phase for the manifestation of incompatibilities, then embryogenesis in Caenorhabditis might be especially susceptible to feeling their effects.…”

“…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 2000;Baird and Seibert 2013;Dey et al 2014), suggesting embryogenesis could be particularly sensitive to disruption in Caenorhabditis and, along with hybrid male sterility (Dey et al 2014), might be among the earliest intrinsic postzygotic barriers to arise during speciation in these organisms. If cell division is a crucial phase for the manifestation of incompatibilities, then embryogenesis in Caenorhabditis might be especially susceptible to feeling their effects.…”

X exceptionalism in Caenorhabditis speciation

“…This hybrid male sterility appears to be caused by X‐autosome incompatibility between these species (Bundus, Wang, & Cutter, ). Substantial recessive incompatibilities reveal themselves in the severe inviability in F2 hybrids of C. remanei and C. latens (F2 hybrid breakdown) (Dey et al., ).…”

“…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., , ).…”