Holocentric repeat landscapes: From micro‐evolutionary patterns to macro‐evolutionary associations with karyotype evolution

Abstract

Repetitive elements can cause large‐scale chromosomal rearrangements, for example through ectopic recombination, potentially promoting reproductive isolation and speciation. Species with holocentric chromosomes, that lack a localized centromere, might be more likely to retain chromosomal rearrangements that lead to karyotype changes such as fusions and fissions. This is because chromosome segregation during cell division should be less affected than in organisms with a localized centromere. The relationships between repetitive elements and chromosomal rearrangements and how they may translate to patterns of speciation in holocentric organisms are though poorly understood. Here, we use a reference‐free approach based on low‐coverage short‐read sequencing data to characterize the repeat landscape of two independently evolved holocentric groups: Erebia butterflies and Carex sedges. We consider both micro‐ and macro‐evolutionary scales to investigate the repeat landscape differentiation between Erebia populations and the association between repeats and karyotype changes in a phylogenetic framework for both Erebia and Carex. At a micro‐evolutionary scale, we found population differentiation in repeat landscape that increases with overall intraspecific genetic differentiation among four Erebia species. At a macro‐evolutionary scale, we found indications for an association between repetitive elements and karyotype changes along both Erebia and Carex phylogenies. Altogether, our results suggest that repetitive elements are associated with the level of population differentiation and chromosomal rearrangements in holocentric clades and therefore likely play a role in adaptation and potentially species diversification.

Polyommatine blue butterflies reveal unexpected integrity of the W sex chromosome amid extensive chromosome fragmentation

“…However, even in our small sample, we also observed considerable differences in genome sizes between and within populations in P. icarus and P. fulgens (Table I). Indeed, study of repeat landscapes in Erebia butterflies showed that repeat composition can vary greatly within species and the variation scales with population divergence (Cornet et al 2023). Further study is needed to confirm whether increase in genome size can be ascribed to activity of horizontally transferred mobile elements (Kandul et al 2004).…”

Macroevolutionary inference of complex modes of chromosomal speciation in a cosmopolitan plant lineage

“…Patterns of repeat DNA— e . g ., LINEs, LTRs, and Helitrons—differ significantly between Carex lineages whose chromosome arrangements evolve at different rates (Cornet et al 2023). Moreover, repeat regions in Carex genomes investigated correlate with chromosome breakpoints across deep phylogenetic breaks as well as within species (Escudero, Marques, Lucek & Hipp 2023, Höök et al 2023), pointing to a mechanism by which natural selection could operate on the genome architecture of chromosome rearrangements in the genus.…”

ZW sex chromosome structure in Amborella trichopoda

“…S11). Moreover, to assess genome-wide repeat expansion across the major Transposable Element (TE) superfamilies 40 , we used repeat landscapes, which showed a comparable pattern within the Z/W (Fig. 3, S12).…”