The wild sex lives of lice: sex ratio distortion in Liposcelis

I think this is my first new thread here, so I just wanted to clarify my intentions regarding this and (hopefully) future posts. I love talking about biology, evolutionary biology in particular, so whenever I find the time (and motivation!), I’m going to attempt to post about papers that caught my attention in hopes that I can spark a discussion that will be educational and entertaining for all of us. Kinda of like an online journal club.

One of my favorite topics in biology concerns the many ways in which the presence of sex and recombination enables “selfish” genetic elements to create conflict within the genome. These conflicts include the spread of transposable elements, meiotic drive, segregation distortion, and lots of other phenomena.

This morning, during a seminar, I presented on a paper concerning the role of meiotic drive in promoting reproductive isolation between closely related species. And just now I happened to come across a recent paper talking about another bizarre sex-related selfish genetic phenomenon. In this case, it’s a species of louse in which some of the females “cheat” the normal rules of mendelian inheritance by never producing males. I thought this might be an interesting topic discussion, and the paper seems to be open access, so without further ado:

Genetics and Genomics of an Unusual Selfish Sex Ratio Distortion in an Insect

Abstract:

Diverse selfish genetic elements have evolved the ability to manipulate reproduction to increase their transmission, and this can result in highly distorted sex ratios [1]. Indeed, one of the major explanations for why sex determination systems are so dynamic is because they are shaped by ongoing coevolutionary arms races between sex-ratio-distorting elements and the rest of the genome [2]. Here, we use genetic crosses and genome analysis to describe an unusual sex ratio distortion with striking consequences on genome organization in a booklouse species, Liposcelis sp. (Insecta: Psocodea), in which two types of females coexist. Distorter females never produce sons but must mate with males (the sons of nondistorting females) to reproduce [3]. Although they are diploid and express the genes inherited from their fathers in somatic tissues, distorter females only ever transmit genes inherited from their mothers. As a result, distorter females have unusual chimeric genomes, with distorter-restricted chromosomes diverging from their nondistorting counterparts and exhibiting features of a giant non-recombining sex chromosome. The distorter-restricted genome has also acquired a gene from the bacterium Wolbachia, a well-known insect reproductive manipulator; we found that this gene has independently colonized the genomes of two other insect species with unusual reproductive systems, suggesting possible roles in sex ratio distortion in this remarkable genetic system.

I have not yet read the paper thoroughly, but here are a few other interesting highlights:

The distorter genome exhibits qualities similar to sex chromosomes:

The inheritance of sex-restricted chromosomes such as the male Y chromosome leads to weakened purifying selection, the accumulation of deleterious mutations, and gene loss. The mode of inheritance and pattern of sequence divergence of distorter-restricted genes suggest that the distorter-restricted genome is in a similar state of deterioration. Consistent with this expectation, although we often observed clear synteny in contig structure, distorter-restricted contigs exhibit divergence from their nondistorter homologs in the form of inversions, indels, and SNPs

It’s possible, though not certain, that the sex ratio distortion may be driven by genes that were horizontally transmitted from Wolbachia, a common intracellular parasite:

Of the remaining genes, three related sequences appear to have been acquired at one time from
Wolbachia and expanded in the distorter genome and represent intriguing candidates for involvement in sex ratio distortion. These sequences are encoded in large contigs (∼70–100 kb), are clearly expressed in the polyA-primed mRNA sequencing, and contain putative introns. The function of these genes and their Wolbachia orthologs is not known, although they contain predicted NB-ARC (nucleotide-binding adaptor shared by APAF-1, certain R gene products, and CED-4) and tetratricopeptide repeat domains (Figure S3). We also found that this gene was independently acquired by at least three other insect species (Figure 4), including two with unusual modes of reproduction. We name this gene Odile , for “only daughters in Liposcelis -associated element”. Odile is also the name of the Black Swan from Tchaikovsky’s ballet, Swan Lake ; she tries to steal the prince from her almost-twin, the White Swan.

Can selfish genetic elements help explain the rapid evolution of sex determining systems?

A major question in evolutionary biology is why sex determination systems evolve so rapidly [2, 12]. One of the main hypotheses to explain the dynamic turnover of sex determination systems and sex chromosomes is that it is shaped by conflicts over transmission. Selfish genetic elements that distort sex ratios have been described across a wide range of organisms, including rodents, insects, and flowering plants [2, 13]. Coevolutionary arms races between these elements and the rest of the genome are thought to play a major role in driving transitions in sex determination. Indeed, the study of sex ratio distortion has uncovered some of the most iconic selfish genetic elements, such as PSR, a selfish chromosome that distorts sex ratios in haplodiploid wasps by destroying all of the chromosomes that were inherited alongside it, so that females that fertilize eggs with the sperm of PSR males produce PSR sons anew [16]. Currently, there is great interest in using natural distorting systems, and learning from them, to control pests and disease vectors [17]. Here, we report the discovery of an unusual mode of sex determination and selfish sex ratio distortion in Liposcelis booklice with accompanying profound genomic consequences. While nondistorter females from an as-yet-unnamed species from Arizona produce both sons and daughters, distorter females never produce sons, although they must mate with males (i.e., the sons of nondistorters) in order to reproduce [3]. The genes that distorter females inherit from their fathers are expressed in their somatic tissues but are not transmitted to the next generation. Because they never transmit paternal DNA to the next generation, distorters are essentially parasitizing males.

Thoughts? Questions?

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That is great @davecarlson. Thanks for this find!

How does meiotic drive promote isolation? Is this a general property, or just in specific cases? It sounds like special cases?

Also, is this is situation described in the paper long-term stable or is it transient?

Allan Miller would be very interested in this paper. I will send him a heads up.

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Hi, thanks for the prod! As a general comment, anyone interested in selfish genetic elements might enjoy Genes in Conflict by Burt & Trivers; quite technical but accessible to anyone with a working knowledge of some basic biology.

As to the question of how it promotes isolation, my supposition would be that such mechanisms constrict gene flow. Gene flow is maximal when segregation is 50/50, because gene flow depends on reciprocal recombination. There’s a frog whose name escapes me that has a ‘genome killer’ gene, such that one parental chromosome set is destroyed. That’s effectively 100% distortion. Thus, even though viable hybrids form, no genes flow between populations through them. But even with a less than fully impermeable barrier, drive can provide a constriction, which promotes population divergence even if fitness is unaffected.

In this case, there are a complex set of factors leading to reproductive isolation including genomic rearrangements. However, the gametes from one species that possess the meiotic driving alleles tend to kill the gametes from the other species (through an as-yet unknown mechanism). One consequence of this that in the hybrid, the viable offspring have a high incidence of unusual chromosome numbers, leading to low fertility.

It’s unclear how general this may be, but there are an increasingly large number of examples along similar lines in different organisms.

Regarding the stability of the situation, the authors speculate that there is an arms-race occuring between driver alleles and alleles that suppress it that is really only revealed in the hybrid:

This genetic conflict between meiotic drive loci and their suppressors would set up an evolutionary arms race where both sides must innovate to try to gain an advantage. We predict that such an arms race is occurring within fission yeasts and we are able to observe drive only in the hybrids because the drive suppressors in Sp are incompatible with the driving alleles in Sk . Under this scenario, it is completely possible that in a cross between Sp and another Sp -like isolate, the Sp drive alleles may emerge victorious.

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18€ on Kindle. I’ll check my piggy bank.

Any more thoughts? Did anybody read the paper that was the subject of the OP and have any questions?

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I have noticed this at TSZ too. With technical papers, I suspect it is hard to comment productively if you are a layperson, or if a science professional and the subject is outside your expertise.

I did enjoy reading the paper and thank Dave for posting it.

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Thanks, Alan!

The frog mentioned is probably Rana esculentus. For more about the phenomenon (which also occurs in some salamander species) look up klepton or kleptogamy.

For something (that I think is) weirder look up androgenesis (e.g. in Cupressus), where a pollen sperm cell colonises an egg and kicks out the egg genome - makes brood parasitism look tame.