Co-option of alternate sperm activation programs in the evolution of self-fertile nematodes

Abstract

Self-fertility evolved independently in three species of Caenorhabditis, yet the underlying genetic changes remain unclear. This transition required that XX animals acquire the ability to produce sperm and then signal those sperm to activate and fertilise oocytes. Here, we show that all genes that regulate sperm activation in C. elegans are conserved throughout the genus, even in male/female species. By using gene editing, we show that C. elegans and C. briggsae hermaphrodites use the SPE-8 tyrosine kinase pathway to activate sperm, whereas C. tropicalis hermaphrodites use a TRY-5 serine protease pathway. Finally, our analysis of double mutants shows that these pathways were redundant in ancestral males. Thus, newly evolving hermaphrodites became self-fertile by co-opting either of the two redundant male programs. The existence of these alternatives helps explain the frequent origin of self-fertility in nematode lineages. This work also demonstrates that the new genome-editing techniques allow unprecedented power and precision in evolutionary studies.

Caenorhabditis evolution in the wild

“…Prospects & Overviews .... known, other than some factors controlling sperm activation [81,82]. Given the important roles of seminal fluid constituents for other organisms in modulating fertility, female physiology and behavior, and in their involvement in sexual selection [83], understanding seminal fluid composition, function, and evolution represents an important underexploited area of Caenorhabditis biology.…”

Proteinase K is an activator for the male‐dependent spermiogenesis pathway in Caenorhabditis elegans: Its application to pharmacological dissection of spermiogenesis

“…Previously, only hermaphrodites were considered to require the spe‐8 class genes during C. elegans spermiogenesis, because spe‐8 class mutant males were fertile. Ancestral dioecious nematode species presumably had two redundant pathways for spermiogenesis in males (Baldi, Cho, & Ellis, ; Wei et al, ). So, perhaps the SPE‐8 class‐dependent pathway evolved from one that initially functioned exclusively in males to one that functioned primarily, but not exclusively, in hermaphrodites.…”

“The persistence of memory”—Hermaphroditism in nematodes

“…Hermaphrodite spermatogenesis is essential for self‐fertility, but not sufficient. Both C. remanei and C. nigoni females have been induced to make sperm in addition to oocytes by knocking down tra‐2 activity, but neither strain became self‐fertile (Baldi et al, ; Wei et al, ). The spermatids of these modified females remained round and inactive, whereas hermaphrodite sperm extend pseudopods and crawl towards oocytes.…”

“…Why do C. elegans hermaphrodites only use the SPE‐8 system for sperm activation, whereas males use TRY‐5 as well? Phylogenetic studies show that both systems exist throughout Caenorhabditis , and must have been present in the male/female ancestor (Wei et al, ). Furthermore, mutants produced by gene editing confirm that these systems are redundant in C. briggsae males, just as they are in C. elegans .…”

“…A few studies have used RNA interference to extend this work to male/female species. In particular, we know that tra-2 (Haag and Kimble, 2000), fem-3 (Haag et al, 2002), and fog-3 (Chen et al, 2001) have conserved functions in Caenorhabditis remanei, as do tra-2 (Wei et al, 2014) and fog-3 (Ting et al, 2014) in Caenorhabditis nigoni. Since C. nigoni is so closely related to C. briggsae that the two can mate and produce some male and female offspring (Woodruff et al, 2010;Kiontke et al, 2011), the rest of the pathway must be roughly conserved as well.…”