The Evolution and Suppression of Male Suicide Under Paternal Genome Elimination

Ross, Laura; Shuker, David M.; Pen, Ido

doi:10.1111/j.1558-5646.2010.01148.x

Cited by 10 publications

(15 citation statements)

References 49 publications

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“…Our model provides two non-mutually exclusive explanations for this. First, once PGE has evolved, the paternally derived genes are under strong selection to evolve counteradaptations (Herrick & Seger 1999;Ross et al 2010b). To avoid this, the maternal or maternally derived genes are selected to either: disable the paternal genome, leading to whole-genome heterochromatisation, as seen in scale insects and beetles; or else completely eliminate it, leading to embryonic PGE, as seen in mites and armoured scale insects.…”

Section: Germline Vs Embryonic Genome Eliminationmentioning

confidence: 99%

Mating ecology explains patterns of genome elimination

Gardner

Ross

2014

Ecology Letters

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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.

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Section: Germline Vs Embryonic Genome Eliminationmentioning

confidence: 99%

Mating ecology explains patterns of genome elimination

Gardner

Ross

2014

Ecology Letters

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“…PGE taxa share the same genetic relationships between relatives as those found in true haplodiploids, but unlike in classic haplodiploidy males are still diploid and carry a complete haploid copy of their father's genome, which is not transmitted to the offspring. As a result, there might be conflict between maternally-and paternally-inherited alleles over transmissionand over male fitness in scenarios of sibling competition, as paternally-inherited alleles in males might favour the fitness of female relatives over their own (Ross et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

“…This process takes place during embryogenesis, and, as a result, males are thought to become functionally haploid, only expressing maternal alleles (Prantera and Bongiorni, 2012) . Like other cases of parent-of-origin specific gene expression, such as genomic imprinting of single genes in mammals and flowering plants (Reik and Walter, 2001;Ferguson-Smith, 2011) , this is thought to result from intragenomic conflict between maternally and paternally derived alleles: silencing of the paternal genome in males could prevent it from expressing anti-PGE adaptations to escape elimination and restoring fair Mendelian transmission or from reducing male fitness under sibling competition (Herrick and Seger, 1999;Ross et al, 2010Ross et al, , 2011 . Although paternal genome silencing has evolved repeatedly in the context of PGE, the hypothesis that it has evolved as an outcome of genomic conflict remains to be tested.…”

Section: Introductionmentioning

confidence: 99%

“…Previous work suggesting the completely silenced state of the paternal genome relied on cytogenetic observations or expression of a small number of phenotypic traits or genetic markers (Brown and Nur, 1964;Brown and Wiegmann, 1969;Brown, 1972;Brun et al, 1995;Borsa and Kjellberg, 1996) , and therefore lack the genome-wide resolution to address this question. Complete silencing of paternally-inherited chromosomes would indicate that there is very little scope of ongoing intragenomic conflict within mealybug males; however, any genes that escape silencing might be involved in conflict (Herrick and Seger, 1999;Ross et al, 2010Ross et al, , 2011 . Second, is paternal genome silencing restricted to somatic tissue, or does it also occur in the germline?…”

Section: Introductionmentioning

confidence: 99%

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Males that silence their father’s genes: genomic imprinting of a complete haploid genome

Filia

Mongue

Dorrens

et al. 2020

Preprint

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Genetic conflict is considered a key driver in the evolution of new reproductive and sex determining systems. In particular, reproductive strategies with non-Mendelian inheritance, where parents do not contribute equally to the genetic makeup of their offspring. One of the most extraordinary examples of non-Mendelian inheritance is paternal genome elimination (PGE), a form of haplodiploidy which has evolved repeatedly across arthropods. Under PGE, males are diploid but only transmit maternally-inherited chromosomes to their offspring, while the paternal homologues are excluded from sperm. This asymmetric inheritance is thought to have evolved through an evolutionary arms race between paternal and maternal genomes over transmission to future generations. In several clades with PGE, such as the mealybugs (Hemiptera: Pseudococcidae), paternal chromosomes are not just eliminated from sperm, but also heterochromatinised early in development and thought to remain inactive. Such paternal genome silencing could alleviate genetic conflict between paternal alleles over transmission.However, it is unclear if paternal chromosomes are indeed genetically inert in both soma and germline. Here, we present a parent-of-origin allele-specific transcriptome analysis in male mealybugs. We show that expression is globally biased towards the maternal genome, but detect activity of paternal chromosomes in both somatic and reproductive tissues. Up to 70% of somatically-expressed genes are to some degree paternally-expressed. However, paternal genome expression is much more restricted in the testis, with only 20% of genes showing paternal contribution. Finally, we show that the patterns of parent-of-origin-specific gene expression are remarkably similar across genotypes and that those genes with biparental expression show elevated rates of molecular evolution. Our results provide the clearest example yet of genome-wide genomic imprinting (parent-of-origin specific gene expression) in insects. Furthermore, it enhances our understanding of PGE, which will aid future empirical tests of evolutionary theory regarding the origin of this unusual reproductive strategy.

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“…"Parahaploidy" is described as a ploidy of the chromosomes, differing from true "haploidy" in males, which the haploid males are derived from haploid eggs (Hartl & Brown, 1970). "Paternal genome loss (PGL)" is a phenomenon of chromosome behavior and is divided into two classes, embryonic PGL and germ-line PGL (Ross et al, 2010b). In embryonic PGL, the paternal genome is eliminated during early embryonic development of males and is found in some armored scale insects.…”

Section: (A) (B)mentioning

confidence: 99%