Mating ecology explains patterns of genome elimination

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.

Intragenomic Conflict over Dispersal

“…In the context of our simple demographically explicit model, the expectation that maternal-origin genes will win the intragenomic conflict at dispersal-promoter loci while paternal-origin genes will win the intragenomic conflict at dispersal-inhibitor loci suggests that the resulting rate of dispersal may be biased toward the interests of the corresponding party if dispersal loci are predominantly promoters or predominantly inhibitors and that the interests of maternal-origin and paternal-origin genes will more or less cancel out in the aggregate if equal numbers of promoters and inhibitors underpin dispersal (Grafen 2006;Gardner and Ross 2014). Moreover, our model predicts that allelic variation segregating at such loci may have relatively large and parent-of-origin-dependent phenotypic effects.…”

How to make a haploid male

“…Rather than specify the number of foundresses on each patch and their fecundities directly, we instead denote by a the probability that any two eggs chosen at random from the same patch were laid by the same foundress. In a departure from Gardner and Ross's () model, we consider that although most eggs are fertilized and develop as viable diploid offspring with sex dependent on the details of the SD mechanism, a vanishing proportion of eggs remain unfertilized and develop as viable haploid male offspring with probability 1‐ c , where c is the viability cost of haploidy. Viable offspring mate at random within their patch, with each female mating with a large number of males.…”

“…We have done so by combining information about the mating systems of haplodiploid clades as well as their diploid sistergroups. We surveyed a number of different aspects of species’ mating system (see Table and Gardner and Ross ) that together allow us to classify each clade as being “frequently inbreeding”, “facultatively inbreeding” or “primarily outbreeding”. We find that inbreeding (either frequent or facultative) is common in most haplodiploid clades.…”

“…The innermost ring depicts GSD systems (with male heterogamety in blue and female heterogamety in red). The outer ring depicts haplodiploid and related SD systems (with dark green depicting “true” haplodiploidy (arrhenotoky), light green depicting “Paternal genome elimination, PGE” where males develop from fertilized eggs but lose their paternal genome during development (Gardner and Ross ) and olive green depicting species with haploid males that could either result from PGE or arrhenotoky. (B) Cladogram of all haplodiploid (arrhenotokous) clades and their diploid sistergroups.…”

Probing the Depths of Biological Diversity During the Second Century ofGENETICS

“…Some species have haploid males and diploid females (e.g., Hymenoptera). Some species start their lives at one ploidy level and end at another (e.g., paternal genome elimination; Gardner and Ross 2014). Why?…”