Mating ecology explains patterns of genome elimination.

Andy Gardner,Laura Ross

doi:10.1111/ele.12383

Abstract

Genome elimination – whereby an individual discards chromosomes inherited from one parent, and transmits only those inherited from the other parent – is found across thousands of animal species. It is more common in association with inbreeding, under male heterogamety, in males, and in the form of paternal genome elimination. However, the reasons for this broad pattern remain unclear. We develop a mathematical model to determine how degree of inbreeding, sex determination, genomic location, pattern of gene expression and parental origin of the eliminated genome interact to determine the fate of genome-elimination alleles. We find that: inbreeding promotes paternal genome elimination in the heterogametic sex; this may incur population extinction under female heterogamety, owing to eradication of males; and extinction is averted under male heterogamety, owing to countervailing sex-ratio selection. Thus, we explain the observed pattern of genome elimination. Our results highlight the interaction between mating system, sex-ratio selection and intragenomic conflict.

Highlights

Under standard mendelian inheritance, individuals receive one set of chromosomes from each of their parents, and transmit one set of chromosomes to each of their offspring, without bias according to each chromosome’s parent of origin
There is a clear pattern in the incidence and type of GE that occurs in the animal kingdom: it is commonly found in association with inbreeding, under male heterogamety, in males, and in the form of paternal genome elimination (Table 1 and Fig. 1)
We assess the impact of the degree of inbreeding, mode of sex determination, genomic location, pattern of gene expression and parental origin of the eliminated genome on the

Summary

Introduction

Individuals receive one set of chromosomes from each of their parents, and transmit one set of chromosomes to each of their offspring, without bias according to each chromosome’s parent of origin. There is a clear pattern in the incidence and type of GE that occurs in the animal kingdom: it is commonly found in association with inbreeding, under male heterogamety, in males, and in the form of paternal genome elimination (Table 1 and Fig. 1) This suggests that a species’ mating ecology is an important factor in predisposing it to GE. A rich literature spanning a century of work in ecology, population genetics and cytology has yielded several hypotheses as to how inbreeding impacts upon the evolution of GE, both directly and in its interaction with a species’ sex determination system (Table 2) These ideas lead to different – sometimes diametrically opposite – predictions, and the complexity of the problem means that a full, quantitative analysis is lacking (Bull 1983; Burt & Trivers 2006)

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