Volumes 159–160, June–July 2024, Pages 66-73Author links open overlay panel, Abstract

B chromosomes are intriguing “selfish” genetic elements, many of which exhibit higher-than-Mendelian transmission. This perspective highlights a group of B chromosomes known as Paternal Sex Ratio chromosomes (PSRs), which are found in several insects with haplo-diploid reproduction. PSRs harshly alter the organism’s reproduction to facilitate their own inheritance. A manifestation of this effect is the conversion of female destined individuals into males. Key to this conversion is the mysterious ability of PSRs to cause elimination of the sperm-inherited half of the genome during zygote formation. Here we discuss how PSRs were discovered, what is known about how they alter paternal chromatin dynamics to cause sex conversion, and how PSR-induced genome elimination is different from other forms of programmed genome elimination in different insects. PSRs also stand out because their DNA sequence compositions differ in remarkable ways from their insect’s essential chromosomes, a characteristic suggestive of interspecies origins. Broadly, we also highlight poorly understood aspects of PSR dynamics that need to be investigated.

Section snippetsSome B chromosomes selfishly disrupt organismal reproduction for transmission

As it turns out, many, perhaps most, B chromosomes possess the unique ability to transmit themselves from parent to offspring at rates higher than Mendelian rules predict. This ability, termed drive, is a distinguishing feature of B chromosomes, and it offsets their tendency to be lost because they are non-essential and cause harm. Although the mechanisms of B chromosome drive (B drive) are diverse, there are some common characteristics. B drive occurs in the germ cell lineage, during the cell

PSR: A sex ratio-distorting B chromosome

PSR was first detected in the jewel wasp, Nasonia vitripennis. It is in this insect that much of what is currently known about PSR was uncovered, and for this reason, most of our discussion will center on PSR in N. vitripennis. A parasitoid belonging to the order Hymenoptera (including all ants, bees, and wasps), N. vitripennis and the flesh fly species that it parasitizes, are found across the temperate regions of the northern hemisphere [15]. Normally, mated female wasps lay progeny broods

The male-biasing effect stems from paternal genome elimination

How does PSR bias the sex ratio toward males? Consideration of this question requires brief mention of the normal chromosomal constituency of the sexes in the jewel wasp. Around 80% of eggs laid by N. vitripennis females are fertilized. These eggs, which have two chromosome sets, one from each parent, develop as females. The remaining unfertilized eggs, which have only a single chromosome set from the female parent, develop as males (Fig. 1). This type of reproduction is referred to as

PSR causes extensive alteration of the sperm’s chromatin

The completeness of paternal genome elimination is critical to (i) ensure PSR’s transmission and (ii) simultaneously preserve insect fitness. As stated previously, the sex of a given individual wasp corresponds to its ploidy level at fertilization. However, the actual mechanism of sex determination begins with a single gene, wasp overruler of masculinization (wom). This gene is imprinted in the female germ line so that the egg’s allele is transcriptionally silenced, while in the male germ line,

How does PSR target other chromosomes (but not itself) for elimination?

One of the more mysterious aspects of PSR is the fact that, while it causes complete paternal genome elimination, this B chromosome does not succumb to its own genome elimination activity. What is the basis of the genome elimination activity? And how is PSR spared from being eliminated during the first mitotic division? This latter question is an especially intriguing one given that PSR resides in the same nucleus with the paternal chromatin until the embryo’s first mitotic division, when

Is PSR’s genome elimination like developmentally programmed events in other insects?

Several insects undergo some form of paternal genome elimination or silencing that is a part of their normal development (reviewed in detail in [36]). For example, in fungus gnats, one or two paternal X chromosomes are eliminated during the mitotic cleavage divisions, while the paternal autosomes (non-sex chromosomes) are discarded during the first meiotic division. In other insects, including mealybugs and booklice, the paternal genome is not discarded but instead transcriptionally silenced

The out-of-Nasonia origin of PSR

Another intriguing feature of PSR is its origin. Of multiple B chromosomes that have been examined in other organisms, many appear to share sequence similarity with certain A chromosomal regions of those same organisms [39], [40]. For this reason, it is held that B chromosomes commonly arise from within their resident species. Previous studies strongly argue that this is not the case for PSR. Early work examining PSR’s sequence composition utilized BAC clones carrying large pieces of DNA from

PSRs in other insects

It is expected that PSRs will thrive in any haplo-diploid species with a sex ratio that is strongly female-biased because, in those species, paternal genome elimination would lead to high levels of PSR-carrying and -transmitting males [14]. Thus, PSRs should not be restricted to the jewel wasp. Indeed, a second PSR was identified in Trichogramma kaykai, a diminutive wasp that resides in the Mojave Desert of the United States and parasitizes the eggs of different butterflies [56], [57].

Concluding remarks: Genome elimination-inducing B chromosomes as outliers among B chromosomes

In summary, PSRs comprise a unique class of B chromosomes. Although there are numerous examples of B chromosomes that exhibit some form of drive, PSRs are exemplars extreme in this regard; their drive involves harshly manipulating organismal reproduction – inducing paternal genome elimination and conversion of female-destined embryos into males – effects that facilitate B chromosome transmission. Indeed, paternal genome elimination is essential, for without it, PSRs would not persist. And this

Declaration of Competing Interest

The authors declare that there are no competing conflicts of interest of any type in the production of this manuscript.

Acknowledgements

We would like to thank J. H. Werren for helpful comments on the manuscript. The work was supported by a grant from the U. S. National Science Foundation (MCB-2127460) awarded to P. M. Ferree.

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