{"title":"Chromosomal conservatism vs chromosomal megaevolution: enigma of karyotypic evolution in Lepidoptera.","authors":"Elena A Pazhenkova, Vladimir A Lukhtanov","doi":"10.1007/s10577-023-09725-9","DOIUrl":null,"url":null,"abstract":"<p><p>In the evolution of many organisms, periods of slow genome reorganization (= chromosomal conservatism) are interrupted by bursts of numerous chromosomal changes (= chromosomal megaevolution). Using comparative analysis of chromosome-level genome assemblies, we investigated these processes in blue butterflies (Lycaenidae). We demonstrate that the phase of chromosome number conservatism is characterized by the stability of most autosomes and dynamic evolution of the sex chromosome Z, resulting in multiple variants of NeoZ chromosomes due to autosome-sex chromosome fusions. In contrast during the phase of rapid chromosomal evolution, the explosive increase in chromosome number occurs mainly through simple chromosomal fissions. We show that chromosomal megaevolution is a highly non-random canalized process, and in two phylogenetically independent Lysandra lineages, the drastic parallel increase in number of fragmented chromosomes was achieved, at least partially, through reuse of the same ancestral chromosomal breakpoints. In species showing chromosome number doubling, we found no blocks of duplicated sequences or duplicated chromosomes, thus refuting the hypothesis of polyploidy. In the studied taxa, long blocks of interstitial telomere sequences (ITSs) consist of (TTAGG)<sub>n</sub> arrays interspersed with telomere-specific retrotransposons. ITSs are sporadically present in rapidly evolving Lysandra karyotypes, but not in the species with ancestral chromosome number. Therefore, we hypothesize that the transposition of telomeric sequences may be triggers of the rapid chromosome number increase. Finally, we discuss the hypothetical genomic and population mechanisms of chromosomal megaevolution and argue that the disproportionally high evolutionary role of the Z sex chromosome can be additionally reinforced by sex chromosome-autosome fusions and Z-chromosome inversions.</p>","PeriodicalId":2,"journal":{"name":"ACS Applied Bio Materials","volume":null,"pages":null},"PeriodicalIF":4.6000,"publicationDate":"2023-06-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"ACS Applied Bio Materials","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1007/s10577-023-09725-9","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"MATERIALS SCIENCE, BIOMATERIALS","Score":null,"Total":0}
引用次数: 0
Abstract
In the evolution of many organisms, periods of slow genome reorganization (= chromosomal conservatism) are interrupted by bursts of numerous chromosomal changes (= chromosomal megaevolution). Using comparative analysis of chromosome-level genome assemblies, we investigated these processes in blue butterflies (Lycaenidae). We demonstrate that the phase of chromosome number conservatism is characterized by the stability of most autosomes and dynamic evolution of the sex chromosome Z, resulting in multiple variants of NeoZ chromosomes due to autosome-sex chromosome fusions. In contrast during the phase of rapid chromosomal evolution, the explosive increase in chromosome number occurs mainly through simple chromosomal fissions. We show that chromosomal megaevolution is a highly non-random canalized process, and in two phylogenetically independent Lysandra lineages, the drastic parallel increase in number of fragmented chromosomes was achieved, at least partially, through reuse of the same ancestral chromosomal breakpoints. In species showing chromosome number doubling, we found no blocks of duplicated sequences or duplicated chromosomes, thus refuting the hypothesis of polyploidy. In the studied taxa, long blocks of interstitial telomere sequences (ITSs) consist of (TTAGG)n arrays interspersed with telomere-specific retrotransposons. ITSs are sporadically present in rapidly evolving Lysandra karyotypes, but not in the species with ancestral chromosome number. Therefore, we hypothesize that the transposition of telomeric sequences may be triggers of the rapid chromosome number increase. Finally, we discuss the hypothetical genomic and population mechanisms of chromosomal megaevolution and argue that the disproportionally high evolutionary role of the Z sex chromosome can be additionally reinforced by sex chromosome-autosome fusions and Z-chromosome inversions.
在许多生物的进化过程中,缓慢的基因组重组时期(= 染色体保守主义)会被大量染色体变化的爆发期(= 染色体大进化)打断。利用染色体级基因组组装的比较分析,我们研究了蓝蝴蝶(Lycaenidae)的这些过程。我们证明,染色体数目保守阶段的特点是大多数常染色体的稳定和性染色体 Z 的动态进化,由于常染色体和性染色体的融合,产生了 NeoZ 染色体的多种变体。相反,在染色体快速进化阶段,染色体数目的爆炸性增长主要是通过简单的染色体裂解实现的。我们的研究表明,染色体大进化是一个高度非随机的渠化过程,在两个系统发育上独立的丽桑花品系中,染色体片段数量的急剧平行增长至少部分是通过重复使用相同的祖先染色体断点实现的。在染色体数目加倍的物种中,我们没有发现重复序列或重复染色体块,因此驳斥了多倍体假说。在所研究的类群中,长的间隙端粒序列(ITSs)块由 (TTAGG)n 阵列与端粒特异性逆转录子穿插组成。ITSs零星地存在于快速进化的莱桑德拉核型中,但不存在于具有祖先染色体数目的物种中。因此,我们推测端粒序列的转座可能是染色体数目快速增加的诱因。最后,我们讨论了染色体巨型进化的假定基因组和种群机制,并认为性染色体-自体融合和 Z 染色体倒位可以进一步加强 Z 性染色体在进化中不成比例的高作用。