Genetic Flexibility in the Convergent Evolution of Hermaphroditism in Caenorhabditis Nematodes

Abstract

The self-fertile hermaphrodites of C. elegans and C. briggsae evolved from female ancestors by acquiring limited spermatogenesis. Initiation of C. elegans hermaphrodite spermatogenesis requires germline translational repression of the female-promoting gene tra-2, which allows derepression of the three male-promoting fem genes. Cessation of hermaphrodite spermatogenesis requires fem-3 translational repression. We show that C. briggsae requires neither fem-2 nor fem-3 for hermaphrodite development, and that XO Cb-fem-2/3 animals are transformed into hermaphrodites, not females as in C. elegans. Exhaustive screens for Cb-tra-2 suppressors identified another 75 fem-like mutants, but all are self-fertile hermaphrodites rather than females. Control of hermaphrodite spermatogenesis therefore acts downstream of the fem genes in C. briggsae. The outwardly similar hermaphrodites of C. elegans and C. briggsae thus achieve self-fertility via intervention at different points in the core sex determination pathway. These findings are consistent with convergent evolution of hermaphroditism, which is marked by considerable developmental genetic flexibility.

Independent recruitments of a translational regulator in the evolution of self-fertile nematodes

“…Cbr-gld-1(nm68) was identified in PCR-based deletion screens (12). Microscopy and immunohistochemistry were performed according to standard methods (SI Materials and Methods).…”

“…In Caenorhabditis nematodes, self-fertile hermaphrodites evolved independently from females in Caenorhabditis elegans and Caenorhabditis briggsae (11)(12)(13)(14). Selfing is an important reproductive adaptation that profoundly affects the efficacy of natural selection (15), population genetic variation (16)(17)(18), and genome content (19).…”

Patterns of Nucleotide Polymorphism Distinguish Temperate and Tropical Wild Isolates of Caenorhabditis briggsae

“…Morphologically, these two species are exceedingly similar, with only subtle differences in traditional systematic characters, such as morphology of the male tail and excretory pore (Nigon and Dougherty 1949;Fitch and Emmons 1995;Baird 2001;Wang and Chamberlin 2002;Félix 2004), despite an estimated divergence of many millions of years (Coghlan and Wolfe 2002;Stein et al 2003). C. briggsae shares the same selfing mode of reproduction as C. elegans and is androdioecious, although phylogenetic analyses and the molecular genetics of sex determination argue that the similar mating systems probably evolved independently (Kiontke et al 2004;Nayak et al 2005;Hill et al 2006). These two species also have partially sympatric geographic distributions and were isolated together on several occasions, although species ranges are poorly characterized in both species.…”

Global Population Genetic Structure of Caenorhabditis remanei Reveals Incipient Speciation

“…It now also serves as a model to study evolutionary transitions in the mode of reproduction (Braendle and Felix 2006;Haag 2009), with several species having evolved self-fertile hermaphroditism (androdioecy) from male-female (gonochoristic) ancestors, including C. elegans (reviewed in Kiontke et al 2004Kiontke et al , 2011Hill et al 2006;Denver et al 2011). Although it is uncertain when selfing arose within each lineage, current evidence suggests that the origin of selfing might be relatively recent Rane et al 2010), implying that the majority of the time separating extant selfing species from outcrossing relatives must have occurred in the ancestral, gonochoristic state.…”