Genomic diversity landscapes in outcrossing and selfing Caenorhabditis nematodes

Abstract

Caenorhabditis nematodes form an excellent model for studying how the mode of reproduction affects genetic diversity, as some species reproduce via outcrossing whereas others can self-fertilize. Currently, chromosome-level patterns of diversity and recombination are only available for self-reproducing Caenorhabditis, making the generality of genomic patterns across the genus unclear given the profound potential influence of reproductive mode. Here we present a whole-genome diversity landscape, coupled with a new genetic map, for the outcrossing nematode C. remanei. We demonstrate that the genomic distribution of recombination in C. remanei, like the model nematode C. elegans, shows high recombination rates on chromosome arms and low rates toward the central regions. Patterns of genetic variation across the genome are also similar between these species, but differ dramatically in scale, being tenfold greater for C. remanei. Historical reconstructions of variation in effective population size over the past million generations echo this difference in polymorphism. Evolutionary simulations demonstrate how selection, recombination, mutation, and selfing shape variation along the genome, and that multiple drivers can produce patterns similar to those observed in natural populations. The results illustrate how genome organization and selection play a crucial role in shaping the genomic pattern of diversity whereas demographic processes scale the level of diversity across the genome as a whole.

Hill-Robertson interference may bias the inference of fitness effects of new mutations in highly selfing species

“…Interestingly, direct measurements of fitness-related traits in mutation accumulation lines suggest that C. elegans has a highly deleterious DFE, with estimates of the mean deleterious selection coefficient ranging from -0.09 to -0.46 (Vassilieva et al 2000;Baer et al 2005;Katju et al 2015). Thus, using previously calculated C. elegans 𝑁𝑁 𝑒𝑒 ranging from 5,000 to 80,000 (Table 4 in Teterina et al 2023), the expected 2𝑁𝑁𝐵𝐵𝑠𝑠 𝑑𝑑 ��� would range from 900 to 72,000, consistent with this explanation. However, there are a few major caveats to these observations.…”

“…elegans is that the true selfing rate in wild C. elegans might be lower than 99%, thus reducing linked effects of selection (Figure 1). Though selfing rate estimates from unique populations range from 80% to ~100% using various methods (Barrière and Félix 2005 elegans estimated a much higher selfing rate of 93%, suggesting that selfing rate can vary across populations (Teterina et al 2023). Importantly, as the samples used in Gilbert et al (2022) were unevenly sampled worldwide (with many samples from Hawaiian populations), variation in selfing rate across populations or through time could additionally influence DFE inference results.…”

“…(3) If possible, it could be extremely helpful to infer the DFE in closely related nonselfing species or in different populations of the same species with known differences in selfing rates. For instance, C. elegans and A. thaliana populations vary in the estimated rates of selfing by ~10%, and the mostly outcrossing A. lyrata has several populations that have evolved partial selfing (Mable et al 2005;Bomblies et al 2010;Teterina et al 2023). Though differences such as population structure and demography need to be carefully accounted for, such comparisons across populations/species could also be used to approximate the extent of HRI in a selfing species.…”

“…Sivasundar and Hey 2005;Teterina et al 2023), in general, the strong LD in C. elegans populations (haplotype blocks of 2.5 Mb on average; Cutter 2006) along with low frequency of males in wild specimens(Barrière and Félix 2005;Richaud et al 2018) suggest the outcrossing rate is very low in most populations. A recent study using whole-genome sequencing data focusing on Hawaiian C.…”

“…Of course, the extent of HRI in these species would likely differ due to differences in outcrossing rates, population sizes, mutation and recombination rates, and the genome architecture(McVean and Charlesworth 2000;Comeron and Kreitman 2002;Kaiser and Charlesworth 2009;Good et al 2014). For instance, the rates of LD decay in the outcrossing species C. remanei and A. lyrata (1-2 kb;Ross-Ibarra et al 2008;Teterina et al 2023) are much higher than the rates in C. elegans and A. thaliana, but the rate of decay is significantly smaller in C. elegans where a complete decay of LD occurs over several Mb(Cutter 2006; Rockman and Kruglyak 2009) compared to A. thaliana (10-50 kb;Ross-Ibarra et al 2008;Shimizu and Tsuchimatsu 2015), suggesting a higher possibility of HRI affecting DFE inference in C.…”