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. 

Introduction

Population genomics aims to infer the evolutionary forces and historical processes that have shaped genetic variation within species while considering the effects of a range of factors such as natural selection, patterns of reproduction, genome functional organization, mutational and recombinational landscapes, as well as spatial and temporal population dynamics and demographic history. As most of these factors act in combination, it can be challenging to infer evolutionary history using DNA sequence information within natural populations. While many population genetic models incorporate several of these factors [1–4], the enormous complexity of the problem means that there is no single analytical model that encompasses all of these interconnected processes. 

Materials and method

Genetic map for Caenorhabditis remanei

We constructed a genetic map for C. remanei from crosses of 2 inbred strains, PX506 and PX553. Initially, C. remanei isolates were derived from individuals living with terrestrial isopods (Oniscidea) taken from Koffler Scientific Reserve at Jokers Hill, King City, Toronto, Ontario, in October 2008 as described in [177]. Strain PX390 was created from one female mated with 3 males from an isopod. Strain PX393 is from one female and one male from an independent isopod. The strains were propagated for 2–3 generations before freezing. PX506 and PX553 are inbred strains generated from PX390 and PX393, respectively (the parental strain for PX506 was inadvertently specified as PX393 in [75]. To reduce residual heterozygosity, the lines were sib-mated for 28–30 generations before freezing. Nematodes were kept under the standard laboratory conditions according to Brenner [43].

Results

Recombination landscape of C. remanei

To generate the first genetic map for an outcrossing species of Caenorhabditis, C. remanei, we crossed two inbred lines (PX506 and PX553) derived from isolates collected near Toronto, Canada ([75], Fig 1 and S1 Table) and individually genotyped 341 F2 offspring. Of the 1,399,638 polymorphic sites among the parental strains, an average of 106,071 markers were covered by bestRAD-sequencing. Full filtration for informative markers yielded 7,512 total sites across the genome, which in turn were used to construct the genetic map. The total length of the genetic map is 288.72 cM. 

Discussion

The transition from traditional population genetics to molecular population genetics shifted the general analytical framework from alleles at a locus to the nucleotide sequence at a particular site in the genome. The progressive expansion of this framework requires scaling these approaches in the context of broader genome-wide factors such as linkage, recombination, and localized variation in mutation rates, as well as how the impacts of these processes are amplified by population history and structure, and species biology. Attempting to understand the separate and combined impacts of these factors requires comprehensive information about molecular diversity across the genome and a theoretical context in which different alternatives can be rigorously tested. 

Acknowledgments

We thank Rose Reynolds, Timothy Ahearne, Chadwick Smith, Scott Scholz for C. remanei mapping strain generation, Larry Meng for DNA isolation of C. remanei nematodes from the Koffler Scientific Reserve used for population genomic sequencing. Many thanks go to Sean O’rourke and members of Mike Miller’s lab at UC Davis for help with bestRAD sequencing, as well as to Gavin Woodruff, Murillo Rodrigues, Peter Ralph, Andy Kern, and other former and current members of Phillips lab and Kern-Ralph co-lab at the University of Oregon for comments and discussions. We thank the Research Advanced Computing Services team for assistance with the computing cluster Talapas at the University of Oregon and the Genomic Core Facility at the University of Oregon for assistance with library preparation.

Citation: Teterina AA, Willis JH, Lukac M, Jovelin R, Cutter AD, Phillips PC (2023) Genomic diversity landscapes in outcrossing and selfing Caenorhabditis nematodes. PLoS Genet 19(8): e1010879. https://doi.org/10.1371/journal.pgen.1010879

Editor: Ian R. Henderson, University of Cambridge, UNITED KINGDOM

Received: December 28, 2022; Accepted: July 21, 2023; Published: August 16, 2023

Copyright: © 2023 Teterina et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All genomic data generated in this study is available in the Sequence Read Archive (SRA) at NCBI under the accession numbers PRJNA800818 and PRJNA799839. Other data reanalyzed in this study is available under the accession number PRJNA549503. The code used in this work is available at https://github.com/phillips-lab/CR_CE_popgen. Supporting datasets for manuscript available at https://doi.org/10.6084/m9.figshare.23826486.

Funding: This study was funded by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant to ADC, a National Institute of General Medical Sciences of the National Institutes of Health grant (R01 GM096008) to ADC and PCP, and a National Institutes of Health (NIH) MIRA award (R35 GM131838) to PCP. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.