A macroevolutionary role for chromosomal fusion and fission in Erebia butterflies

  1. Hannah Augustijnen
  2. Livio Bätscher
  3. Martin Cesanek
  4. Tinatin Chkhartishvili
  5. Vlad Dincă
  6. Giorgi Iankoshvili
  7. Kota Ogawa
  8. Roger Vila
  9. Seraina Klopfstein
  10. Jurriaan M. de Vos
  11. Kay Lucek

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Abstract

The impact of large-scale chromosomal rearrangements, such as fusions and fissions, on speciation is a long-standing conundrum. We assessed whether bursts of change in chromosome numbers resulting from chromosomal fusion and fission are related to increased speciation rates in Erebia , one of the most species-rich and karyotypically variable butterfly groups. We established a genome-based phylogeny and employed state-dependent birth-death models to infer trajectories of karyotype evolution across this genus. We demonstrated that rates of anagenetic chromosomal changes ( i.e . along phylogenetic branches) exceed cladogenetic changes ( i. e . at speciation events), but when cladogenetic changes occur, they are mostly associated with chromosomal fissions rather than fusions. Moreover, we found that the relative importance of fusion and fission differs among Erebia clades of different ages, where especially in younger, more karyotypically diverse clades, speciation is more frequently associated with chromosomal changes. Overall, our results imply that chromosomal fusions and fissions have contrasting macroevolutionary roles and that large-scale chromosomal rearrangements are associated with bursts of species diversification.

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  1. PREreview

    This Zenodo record is a permanently preserved version of a PREreview. You can view the complete PREreview at https://prereview.org/reviews/7851943.

    Review of the preprint- A macroevolutionary role for chromosomal fusion and fission in Erebia butterflies (Augustijnen et al. 2023) DOI: https://doi.org/10.1101/2023.01.16.524200

    Discussion led by: Mar Repullés (14.04.2023) Notes taken by: Pedro Ribeiro

    Review written by: Participants of Journal Club (Mar Repullés, Prapti Gohil, Nils Schumacher, Daniel Linke, Phil Honle, Petr Klimes, Pavel Matos, Irena Kleckova, Alena Suchackova, Pedro Ribeiro)

    Overview

    In this preprint, the authors investigate the role of changes in chromosome numbers in the speciation rates of butterflies in the Erebia genus. Specifically, they test whether anagenetic or cladogenetic changes are more strongly associated with speciation in the group, and if either fusions or fissions are the driving forces leading to these changes. The preprint is very well written, clear and of potential broad interest in the areas of evolution and chromosomal evolution, and it uses up-to-date methods and data. Nonetheless, we still have a few suggestions, which the authors may find useful to improve the article.

    1) The authors strongly assume that fusions and fissions drive chromosome number changes in these butterflies. We believe this assumption is quite strong and perhaps the authors may mention other processes that may explain extant chromosome number variation. For example, if the assumption holds, we would see the same genome sizes across all Erebia species, despite their variation in chromosome numbers.

    2) Perhaps discuss in more detail the large amount of missing trait data and how it limits the inferences of state-dependent-diversification models (for example, ChromoSSE).

    In the same line, could you please:

    - Explain if the missing data are equally distributed among the species groups and show it more clearly in the figures.

    - mark in the phylogeny (Figure 1, panel C) which of the species have the chromosome data. 

    - In the figure 2, record the species with known number of  chromosomes to easily distinguish them from the estimated extant chromosome numbers as shown in pie charts on the terminal nodes.

    - In the caption of the Figure 1, the chromosome numbers were taken from different study, probably Lucek 2018 (doi:10.3390/genes9030166), not from Peña at al. 2015

    3) The estimation of the age of the Erebia crown group. The divergence times seem to be quite young compared to other publications (e.g. Peña et al. 2015, Kleckova et al. 2023). We believe the reason is behind is the use of secondary calibrations for Nymphalidae from Kawahara et al. (2019), which estimate Nymphalidae crown age to be much younger than other published butterfly phylogenies (e.g., Espeland et al. 2018, Chazot et al. 2021).

    Other suggestions: 

    • We believe that Figure 3 is not really informative for the study and may break the flow of the story. Perhaps it could be added in the supplementary material. 

    Competing interests

    The author declares that they have no competing interests.

  2. Version published to 10.1101/2023.01.16.524200v1 on bioRxiv