Gene family evolution in brassicaceous-feeding insects: Implications for adaptation and host plant range

  1. Nitin Ravikanthachari
  2. Carol L Boggs

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Abstract

Herbivores have a defined range of hostplants that they can feed on, which is mediated by underlying detoxification and sensory repertoires. Insects that feed on Brassicaceae represent one of the striking examples of co-evolutionary arms race. Insects specialized on Brassicaceae have evolved specific mechanisms to detoxify mustard oils (glucosinolates), while generalist species use detoxification enzymes that act on a variety of substrates. Understanding the gene evolution of detoxification and sensory repertoire in specialist and generalist Brassicaceae feeders will shed light on the processes involved in mediating hostplant ranges in herbivores. We use a comparative phylogenomic approach in 12 lepidopterans that feed on Brassicaceae, ranging from specialist to pests in their host range to examine the gene family expansion of detoxification and sensory gene families. We found that gene family expansions and contractions were larger in generalist herbivores compared to specialist herbivores. Gene evolutionary rate of detoxification genes reflected hostplant range where generalists had a higher evolutionary rate of detoxification genes that act on wide substrates while specialists had a higher evolutionary rate in genes that conjugate toxic compounds to hydrophilic byproducts. Our analysis on the nitrile specifier gene, a key innovation for feeding on Brassicaceae, indicated pervasive purifying selection with lineage specific differences in selection. Our results add to the growing body of work addressing gene family evolution and its role in hostplant range and specialization in insects.

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  1. Arcadia Science

    Higher gene family evolution rates could be due to underlying gene duplication, neo-functionalization and/or genome rearrangements, all of which are implicated in polyphagous feeding (Murad et al., 2021; Seppey et al., 2019).

    Horizonal transfer (including introgression following hybridization) is another potential explanation - this would be a good place to discuss this point.

  2. Arcadia Science

    The root of the species tree was time calibrated to 87 Myr to reflect the divergence of the three families used in the analysis (Espeland et al., 2018).

    This needs to be explained further. How exactly was this done? Did you convert the inferred species tree to be ultrametric and then change the root depth to 87Myr? If so, this is not an appropriate method for time-calibration.

    At a minimum, I would suggest either using this root age and r8s as implemented in geiger (https://rdrr.io/cran/geiger/man/r8s.phylo.html), or PATHd8 (https://www2.math.su.se/PATHd8/). Alternatively you could use another species tree time calibrated with other more intensive methods that includes some proportion of these species, and use the congruificaton method (again implemented in geiger (https://rdrr.io/cran/geiger/man/congruify.phylo.html) which uses PATHd8 or treePL under the hood.

    If you've used one of these methods to time calibrate your tree, be sure to describe that here.

  3. Arcadia Science

    We additionally used Orthofinder for constructing our species and gene phylogenetic tree.

    How sensitive might your results be to the inferred species tree topology? Numerous efficient methods exist that are capable of inferring species trees from multiple copy gene families, including asteroid (https://github.com/BenoitMorel/Asteroid) and ASTRAL-Pro2 (https://github.com/chaoszhang/ASTER/blob/master/tutorial/astral-pro.md).

    Additionally, SpeciesRax (https://github.com/BenoitMorel/GeneRax/wiki/SpeciesRax) is capable of inferring a rooted species tree using multi-copy gene family trees (in this respect similar to the STAG algorithm implemented in OrthoFinder) under a model of gene duplication, transfer, and loss.

    I would suggest applying one of these methods to assess how robust your species tree topology is to choice of methods, as the inferred gene family evolutionary dynamics will naturally be sensitive to this.

  4. Arcadia Science

    CAFE v. 5.0 (Mendes et al., 2020) was used to analyze gene family evolution under a phylogenetic framework.

    Could you briefly explain why this approach was chosen rather than species/gene tree reconciliation methods like ALE (https://github.com/ssolo/ALE) or GeneRax (https://github.com/BenoitMorel/GeneRax)?

    Because CAFE only models gene duplications and losses, it's unable to account for or infer potential horizontal gene transfer among your focal species, a process that could (and likely does) explain some proportion of the variation in gene copy number observed in the analyzed gene families.

    I would suggest briefly addressing these points, first in the methods section, and subsequently in the discussion. HGT is a plausible alternative hypothesis to gene duplication, and one that is sensible in the context of gene family-diversity associated increases in a species' capacity for hostplant range expansion.

  5. Arcadia Science

    We additionally filtered OGs that showed high variance across species as they can lead to biases in gene family evolution estimation as well as preventing convergence among replicates in the analysis.

    This makes good sense, though I might suggest elaborating on what sorts of biases high variances might introduce (e.g. 'cascading' influence on inferred expansions on branches neighboring unsusually high copy numbers?).

    Additionally, how exactly did you filter - did you calculate variance among species (or std. deviation for instance) and then filter based on some empirical threshold?

  6. Version published to 10.1101/2023.06.09.544424v1 on bioRxiv