Genomic signatures associated with the evolutionary loss of egg yolk in parasitoid wasps

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Abstract

Trait regression and loss have occurred repeatedly in numerous lineages throughout evolutionary history in response to changing environments. In parasitoid wasps, a mega-diverse group of hymenopteran insects, loss or reduction of yolk in the egg has been reported in many species. This phenotypic change likely evolved as a response to the shift from ectoparasitism to endoparasitism. However, the genetic basis of this trait and the impact of its loss on genome evolution remain poorly understood. Here, we performed a comparative genomic analysis of 64 hymenopteran insects. The conserved insect yolk protein gene vitellogenin ( Vg ) underwent five independent loss events in four families, involving 23 of the analyzed endoparasitoid species. Whole-genome alignment suggested that Vg loss occurred during genome rearrangement events. Analysis of Vg receptor gene ( VgR ) loss, selection, and structural variation in lineages lacking Vg demonstrated functional biases in the patterns of gene loss. The ectoparasitism to endoparasitism transition did not appear to be the primary driver of Vg loss or the subsequent VgR evolution. A number of parallel and convergent genomic changes were observed between Vg -loss lineages, including gene family evolution and selection of genes related to transport, development, and metabolism. These changes may have facilitated embryonic development without the yolk in these lineages. Together, these findings reveal the genomic basis underlying a unique trait loss in parasitoid wasps. More broadly, this study enhances our understanding of yolk loss evolution outside the class Mammalia, highlighting a potential evolutionary trend arising from the availability of an alternative nutrient source for embryonic development.

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  1. Data availability

    Will the code to run these analyses be available on Github? It would be helpful to follow along with the many steps used across these analyses.

  2. Overall, these results revealed dramatic differences between Vgs and PVgs with respect to both evolutionary history and gene expression

    Does this finding then support the previous result that A. japonica lost its yolk?

  3. Together, these results demonstrated parallel or convergent changes in specific gene families in addition to shared gene selection events across five independent Vg-loss lineages. These genomic changes may have been related to adaptation to the endoparasitic lifestyle

    I wonder whether these other genes may be lost in the transition of egg yolk loading to harnessing another organism’s nutrients for development, rather than after? I think I may just not be super clear on how this is able to tell that these changes happened after the loss of Vg.

    This dataset seems like it has the capacity to look at genes beyond Vg and VgR - I would be very curious to see if there are any other genes, especially ones associated with observable phenotypes (e.g., egg size, developmental timeline, features, etc.), that can be interrogated the same way.

  4. The hypothesis for positive selection suggests that yolk loss could save energy costs and increase fecundity76, but this hypothesis has not been directly tested

    I could totally see follow-up experimental work examining fecundity and offspring survival rates in yolkless vs. yolk groups of endoparasitoids!

  5. wasps

    This is a really interesting finding. Do you think there are host traits that may be associated with Vg loss? Maybe certain hosts have "richer" hemolymph, which makes it more likely that a parasitoid will lose its own yolk? Or is it more likely that this is purely a genome rearrangement phenomenon?

  6. fragmented

    On the note of genome assemblies, I really appreciate your inclusion of the metadata in Supplementary Table 11. Out of curiosity, how much do you think the quality of genome assemblies impacts your results more broadly?

  7. wasps

    Why are Vg genes so commonly found at genome rearrangement breakpoints? I don’t know very much about where these rearrangement breakpoints fall, but are there unique genomic factors surrounding these genes that make them more prone to loss?

  8. This revealed a great deal of variation in Vg copy number within the order Hymenoptera

    Are there any interesting patterns with Vg copy number beyond presence/absence? It would be interesting to know more about the multiple copies present in the non-parasitoid hymenopterans. I'm especially curious about multiple copies in parasitoid species - from a quick glance, the only loss events seem to be in species related to those with only one Vg copy.

  9. Genomic data (including genomic sequences and genome annotation results) of 64 representative hymenopteran insects were mainly collected from publicly database, including the National Center for Biotechnology Information (NCBI)79, InsectBase v280, and Darwin Tree of Life Project81. For RNA-seq analysis, we also collected RNA-seq data of 10 species from NCBI Sequence Read Archive (SRA) database. Find details about data collection in Supplementary Table 11.

    I really, really appreciate the use of public data to ask a unique question!