Investigating Phylogenetic Conflict using Homolog Trees reveals the Genetic Basis of Phenotypic Convergence in Carnivorous Sundews

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Abstract

Phenotypic convergence is found across the tree of life, and morphological similarities in distantly related species are often presumed to have evolved independently. However, clarifying the origins of traits has recently highlighted the complex nature of evolution, as apparent convergent features often share similar genetic foundations. Hence, the tree topology of genes that underlie such traits frequently conflicts with the overall history of species relationships. This conflict creates both a challenge for systematists and an exciting opportunity to investigate the rich, complex network of information that connects molecular trajectories with trait evolution. Here we probe the evolutionary history of pleisiomorphic features in the carnivorous Caryophyllales, a charismatic group of flowering plants. Using a novel conflict identification program named CAnDI (Conflict And Duplication Identifier), we dissect all gene relationships within homolog trees and find genomic evidence that the molecular basis of mucilaginous sticky traps was likely present in the ancestor of all carnivorous Caryophyllales. We also show that many genes whose evolutionary trajectories group species with similar trap devices code for proteins contributing to plant carnivory and identify a LATERAL ORGAN BOUNDARY DOMAIN gene as a possible regulator of sticky trap development. Our results demonstrate that analysing conflict on homolog trees, rather than pre-identified orthologs, can aid in uncovering the genetic basis of trait evolution.

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  1. Parsimony-based ancestral state reconstruction was performed on the carnivorous clade of the tree in Mesquite version 3.70 (Maddison and Maddison 2021).

    It surprises me that you've chosen to use parsimony to infer ancestral character states when the rest of this paper and the motivation of the CAnDI software itself is clearly motivated by explicit, formal models of evolution.

    If you were to infer ancestral character states using a Markov model of discrete states, are there major differences in ancestral state reconstructions as compared to the parsimony reconstructions?

    The trait distribution is quite simple (not a lot of within clade trait heterogeneity), but at the very least I might suggest conducting formal model comparison among (for instance) an equal-rates, symmetric / asymmetric rates, and all-rates-different Mk models and reporting the inferred character states under these model and compare them to your parsimony reconstructions. If they are concordant, that's fantastic! But if not, it would be worth commenting on how this might impact your interpretations.

  2. The sequence with the greatest number of characters was retained for each gene while lower-quality duplicates were discarded using a script written in Python (https://github.com/HollyMaeRobertson/treebuilding-scripts/blob/main/remove_repeats.py)

    Can you provide some more specific explanation as to what this script is doing under the hood?

    For instance, what characteristics lead you to classify gene copies as lower quality duplicates? How could these decisions impact or influence your inferences surrounding conflict, and could removal of legitimate but divergent duplicate gene copies bias your results in some way?

  3. conflicts of interest

    I'm not entirely clear what you mean to say with this - could you perhaps use other language to help clarify?

    Do you mean to communicate that the method allows users to identify specific instances or concerted patterns of conflict that are coincident with or predictive of trait evolution?