Academic journal article Genetics

Insights into Species Divergence and the Evolution of Hermaphroditism from Fertile Interspecies Hybrids of Caenorhabditis Nematodes

Academic journal article Genetics

Insights into Species Divergence and the Evolution of Hermaphroditism from Fertile Interspecies Hybrids of Caenorhabditis Nematodes

Article excerpt

ABSTRACT

The architecture of both phenotypic variation and reproductive isolation are important problems in evolutionary genetics. The nematode genus Caenorhabditis includes both gonochoristic (male/female) and androdioecious (male/hermaprodite) species. However, the natural genetic variants distinguishing reproductive mode remain unknown, and nothing is known about the genetic basis of postzygotic isolation in the genus. Here we describe the hybrid genetics of the first Caenorhabditis species pair capable of producing fertile hybrid progeny, the gonochoristic Caenorhabditis sp. 9 and the androdioecious C. briggsae. Though many interspecies F^sub 1^ arrest during embryogenesis, a viable subset develops into fertile females and sterile males. Reciprocal parental crosses reveal asymmetry in male-specific viability, female fertility, and backcross viability. Selfing and spermatogenesis are extremely rare in XX F^sub 1^, and almost all hybrid self-progeny are inviable. Consistent with this, F^sub 1^ females do not express male-specific molecular germline markers. We also investigated three approaches to producing hybrid hermaphrodites. A dominant mutagenesis screen for self-fertile F^sub 1^ hybrids was unsuccessful. Polyploid F^sub 1^ hybrids with increased C. briggsae genomic material did show elevated rates of selfing, but selfed progeny were mostly inviable. Finally, the use of backcrosses to render the hybrid genome partial homozygous for C. briggsae alleles did not increase the incidence of selfing or spermatogenesis relative to the F^sub 1^ generation. These hybrid animals were genotyped at 23 loci, and significant segregation distortion (biased against C. briggsae) was detected at 13 loci. This, combined with an absence of productive hybrid selfing, prevents formulation of simple hypotheses about the genetic architecture of hermaphroditism. In the near future, this hybrid system will likely be fruitful for understanding the genetics of reproductive isolation in Caenorhabditis.

THE genetic basis of phenotypic diversity is an important, albeit poorly understood phenomenon. Caenorhabditis nematodes provide a system that can address such an issue. Caenorhabditis elegans can act as an excellent point of reference for comparative development studies (Félix 2007; Lin et al. 2009; Schulze and Schierenberg 2009), and the variation in reproductive mode within Caenorhabditis is an alluring subject for such investigations (Haag 2005). Some Caenorhabditis species are gonochoristic (male/ female), whereas others are androdioecious (male/ hermaphrodite; Figure 1). Hermaphrodites and females are somatically similar, but while females only make oocytes, hermaphrodites briefly undergo spermatogenesis before switching to oogenesis (Ellis and Schedl 2006). This striking interspecies difference is not only discrete and easily scored, but is also of great consequence for reproductive strategies and population genetics.

Many studies have addressed the evolution of germline sex determination in Caenorhabditis. Phylogenetic analyses suggest that the trait has evolved convergently in this lineage multiple times (Cho et al. 2004; Kiontke et al. 2004). Consistent with this, differences in the presence and functions of germline sex determination genes have been uncovered between the convergently evolved C. elegans and C. briggsae (Nayak et al. 2005;Hill et al. 2006; Guo et al. 2009). Similarities in germline sex determination between gonochoristic and androdioecious Caenorhabditis species have also been found (Haag and Kimble 2000; Chen et al. 2001; Haag et al. 2002). Remarkably, reverse genetic manipulations can cause a C. remanei female to produce activated sperm and lay self-progeny (Baldi et al. 2009). However, despite these successes, there has been little progress in identifying the historical causative genetic differences distinguishing hermaphrodites from their female ancestors. Indeed, because the exact cause of the spermto- oocyte switch in C. …

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