Abstract

Organismal genome sizes vary by six orders of magnitude and appear positively correlated with organismal size and complexity. Neutral models have been proposed to explain the broad patterns of genome size variation based on organism population sizes. In the Caenorhabditis genus, hermaphrodite genomes are smaller than those of gonochoristic species. One possible driving force for this genome size difference could be non-random chromosome segregation. In Caenorhabditis elegans, chromosome assortment is non-independent and violates Mendel’s second law. In males, the shorter homologue of a heterozygous autosome pair preferentially co-segregates with the X chromosome while the longer one preferentially co-segregates with the nullo-X (O) chromosome in a process we call “skew”. Since hermaphrodites preferentially receive the shorter chromosomes and can start populations independently, their genome size would be predicted to decrease over evolutionary time. If skew is an important driver for genome size reduction in hermaphroditic Caenorhabditis species, then it should be present in all congeneric species. In this study, we tested this hypothesis and found that skew is present in all eight examined species. Our results suggest that skew is likely the ancestral state in this genus. More speculatively, skew may drive genome size patterns in hermaphroditic species in other nematodes.

Highlights

  • Why is there variation in genome size amongst organisms? Organismal genome sizes span six orders of magnitude[1,2] from ~160 kb to ~150 Gb

  • We found that the transmission of transgenes preferentially toward sons is present in all Caenorhabditis species tested

  • Skew occurs in C. elegans whereby fathers transmit autosomes that are heterozygous in length to their offspring in a non-Mendelian fashion[17]

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Summary

Introduction

Why is there variation in genome size amongst organisms? Organismal genome sizes span six orders of magnitude[1,2] from ~160 kb (bacterial endosymbiont Carsonella ruddii3) to ~150 Gb (angiosperm, Paris japonica[4]). In the Elegans subgroup of the Caenorhabditis genus, all 3 cases of the evolution of hermaphroditism have been associated with a convergent reduction in genome size relative to gonochoristic (male/female) species[8,9,10,11,12,13]. The gonochoristic species (C. remanei and C. brenneri) have larger population sizes than hermaphroditic species (C. briggsae and C. tropicalis), consistent with the expectations for outcrossing and selfing species[14,15,16]. Gonochoristic species (C. remanei, C. brenneri, C. japonica, C. sinica and C. nigoni) have larger genome sizes than hermaphroditic species (C. elegans, C. briggsae and C. tropicalis)[8,9,10]. Populations of C. elegans are frequently initiated by hermaphrodites[18,19,20,21], skew may partially explain genome size reduction relative to the ancestral gonochoristic species

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