Chromosome evolution in insects

Butterfly chromosomes are holocentric, i.e., lacking a localized centromere. Potentially, this can lead to rapid karyotypic evolution through chromosome fissions and fusions, since fragmented chromosomes retain kinetic activity, while fused chromosomes are not dicentric. However, the actual mechanisms of butterfly genome evolution are poorly understood. Here, we analyzed chromosome-scale genome assemblies to identify structural rearrangements between karyotypes of satyrine butterfly species. For the species pair Erebia ligea-Maniola jurtina, sharing the ancestral diploid karyotype 2n = 56 + ZW, we demonstrate a high level of chromosomal macrosynteny and nine inversions separating these species. We show that the formation of a karyotype with a low number of chromosomes (2n = 36 + ZW) in Erebia aethiops was based on ten fusions, including one autosome-sex chromosome fusion, resulting in a neo-Z chromosome. We also detected inversions on the Z sex chromosome that were differentially fixed between the species. We conclude that chromosomal evolution is dynamic in the satyrines, even in the lineage that preserves the ancestral chromosome number. We hypothesize that the exceptional role of Z chromosomes in speciation may be further enhanced by inversions and sex chromosome-autosome fusions. We argue that not only fusions/fissions but also inversions are drivers of the holocentromere-mediated mode of chromosomal speciation. https://www.mdpi.com/2073-4425/14/2/437

In insects, two types of telomere length maintenance are known: telomerase-dependent, resulting in chromosome ends consisting of short nucleotide repeats (typically TTAGG), and telomerase-independent, resulting in chromosome ends consisting of long nucleotide repeats or transposon-like elements. However, only a few species have been previously studied with regard to their telomere DNA sequences. Here, based on analysis of chromosome-level genome assemblies, I present the data on telomere and subtelomere organization for 180 species from 148 genera, 53 families and 8 orders of insects. Analysis of these taxa reveals that in fact chromosome ends of most insect species have an intermediate structure and consist of numerous arrays of short telomeric repeats interspersed with telomere-specific non-LTR retrotransposons. An unexpectedly high level of diversity of short telomeric motifs (22 variants ranging in length from 1 to 17 nucleotides) is documented. Telomeres consisting of long repeats (from 173 to 374 bp) are confirmed for flies (the order Diptera) and also found in the orders Odonata and Hymenoptera. The most unusual telomere structure is found in the bee Lasioglossum lativentre , in which the chromosomes possess the short telomeric repeat TTAGGTCTGGG at only one end, whereas opposing ends terminate with medium and long repeats. I conclude that different types of telomere organization and numerous variants of long and short T-containing motifs, including the (T) n mononucleotide sequence, are compatible with the performance of telomere functions. I argue that both telomerase-dependent and telomerase-independent mechanisms for maintaining telomere length operate simultaneously in many insects. The balance between them and the exchange of sequences between telomeres and subtelomeres are most likely the key factors that determine the structure and evolution of telomeres. Significance Multilayer telomeres, resulted from numerous, site-specific insertions of retrotransposons into the region of short telomeric repeats, are not an aberrant type of organization, as previously thought. They are widely distributed among insects and can represent up to 30-40 % of eukaryotic species diversity. Accordingly, the telomere maintenance mechanism based on the joint work of telomerase-dependent and telomerase-independent mechanisms can also be extremely widespread in nature.

Стекольников А.А., Иванов В.Д., Кузнецов В.И., Лухтанов В.А.2000. Эволюция хромосомного аппарата, крыловых сочленений, гениталий самцов и филогенез дневных чешуекрылых (Lepidoptera: Hesperioidea, Papilionoidea)// Энтомологическое обозрение. Т. 79, вып. 1. С. 123-149. [A.A.Stekolnikov, V.D.Ivanov, V.I.Kuznetzov, V.A.Lukhtanov (2000) Evolution of chromosomes, wing articulation, male genitalia and phylogeny of butterflies (Lepidoptera: Hesperioidea, Papilionoidea). – Entomologicheskoe obozrenie 79(1):123-149.]

In karyotype of many organisms, chromosomes form two distinct size groups: macrochromosomes and microchromosomes. During cell divisions, the position of the macro-and microchromosomes is often ordered within metaphase plate. In many reptiles, amphibians, birds, insects of the orthopteran family Tettigoniidae and in some plants, a so called "reptilian" type organization is found, with microchromo-somes situated in the center of metaphase plate and with macrochromosomes situated at the periphery. An opposite, "lepidopteran" type is known in butterflies and moths (i.e. in the order Lepidoptera) and is characterized by macrochromosomes situated in the center and by microchromosomes situated at the periphery. The anomalous arrangement found in Lepidoptera was previously explained by holocentric organization of their chromosomes. Here I analyse the structure of meiotic metaphase I plates in ithomi-ine butterfly, Forbestra olivencia (H. Bates, 1862) (Nymphalidae, Danainae, Ithomiini) which has a clear "reptilian" organization, contrary to previous observations in Lepidoptera. In this species large bivalents (i.e. macrochromosomes) form a regular peripheral circle, whereas the minute bivalents (i.e. microchro-mosomes) occupy the center of this circle. The reasons and possible mechanisms resulting in two drastically different spatial chromosome organization in butterflies are discussed.

Karyotypic features of some families of noctuoid and bombycoid complexes.

Text in Russian. English abstract is provided in the uploaded file.

Significance Changes in the number and/or structure of chromosomes (i.e., chromosomal rearrangements) have the potential to drive speciation. However, their accumulation in a population is considered both difficult and unpredictable, because the greatly reduced reproductive fitness of chromosomal hybrids prevents fixation of novel karyotypes. Here, we provide evidence for a mechanism that rescues fertility of chromosomal hybrids in species with holocentric chromosomes. We demonstrate that chromosomal heterozygotes of Leptidea Wood White butterflies have a reverse order of main meiotic events in which the first and most critical stage of the chromosome number reduction is replaced by the less risky stage of sister chromatid separation. This may facilitate long-term persistence of chromosomal rearrangements, which is a major prerequisite for chromosomal speciation.

Mitotic and meiotic chromosomes from 2 taxa of the genus Melinaea, M. satevis cydon and M. "satevis" tarapotensis (Lepidoptera: Nymphalidae), and from hybrids produced in captivity were obtained using an improved spreading technique and were subsequently analyzed. In one of the taxa, the presence of trivalents and tetravalents at diakinesis/metaphase I is indicative of heterozygosity for multiple chromosome fusions or fissions, which might explain the highly variable number of chromosomes previously reported in this genus. Two large and complex multivalents were observed in the meiotic cells of the hybrid males (32 chromosomes) obtained from a cross between M. "s." tarapotensis (28 chromosomes) and M. s. cydon (40-43 chromosomes). The contribution of the 2 different haploid karyotypes to these complex figures during meiosis is discussed, and a taxonomic revision is proposed. We conclude that chromosome evolution is active and ongoing, that the karyotype of the common ancestor consisted of at least 48 chromosomes, and that evolution by chromosome fusion rather than fission is responsible for this pattern. Complex chromosome evolution in this genus may drive reproductive isolation and speciation, and highlights the difficulties inherent to the systematics of this group. We also show that Melinaea chromosomes, classically considered as holocentric, are attached to unique, rather than multiple, spindle fibers.

Analysis of original data (12 species) and data extracted from the literature (203 species) demonstrates that the haploid chromosome number n=31 is the ancestral one for the family Pieridae. This number (n=31) is preserved in the majority of the subfamilies Dismorphiinae, Coliadinae and Anthocharinae, but not in the Pierinae. In the Pierinae, the tribe Eroniini demonstrates n = 16-18, the tribe Teracolini - n = 27-28, the tribe Appiadini -n = 32, and the tribe - Pierini n = 25, 26. The numbers n = 12 and n-=19 are found in the genus Leptosia.

It is established that Dicallomera fascelina sensu auct. is not one species but, rather, a complex of species. Two karyologically distinct species in this complex were detected. The haploid chromosome number for a population of D. fascelina from North Caucasus is found to be 16, while that for D. kusnezovi sp. n. from Wrangel Island situated between the East Siberian and the Chuckchee Seas is 20. These two species also differ in the female genitalia and coloration of caterpillars.

The karyotypes of six species of the genus Agrodiaetus Hübner were studied. The following chromosome numbers were found: n = ca 60-65 in three populations of A. sibirica (Staudinger) stat. n. from the Altai; n = 15, 16 in A. ciscaucasica Forster stat. n. from the Northern Caucasus; n = 22 in A. aserbeidschana aserbeidschana Forster from Talysh; n = 45 in A. damon (Denis & Schiffermüller) from the Altai; n = 19 in A. cyanea (Staudinger) from Armenia and Nakhichevan and n = 33-34 in A. ninae Forster from Armenia. The karyotypes of the first three taxa were studied for the first time, and the first karyological data were obtained for populations of the three latter species in the USSR, including A. ninae in the type locality. It is concluded that A. damone (Eversmann), A. carmon (Herrich-Schäffer) and A. transcaspica (Staudinger) are not polytypic, widely distributed species, but complexes of several species with restricted areas. The taxonomic level, systematic position and distribution of the species are discussed.

In hexapods, unlike the majority of animals, development without fertilization is a common phenomenon. They evolved a striking diversity of unisexual reproductive types that include a variety of modes starting from spontaneous parthenogenesis in females to the production of impaternate males with different variants in between. Many reports about parthenogenetic species have accumulated over time. Here, we present a review of various parthenogenetic hexapod groups with a particular focus on their chromosome systems and ploidy level. We show that conclusions about the reproductive mode often lack solid evidence and sometimes inefficiently demonstrate how parthenogenesis is maintained in corresponding groups. In this review, basal hexapods (Protura, Collembola, Diplura), primarily wingless insect groups (‘Apterygota’) and non-holometabolous insects are listed with references to a variety of their unisexual reproductive modes.

Despite predictions of the classic, hybrid-sterility model of chromosomal speciation, some organisms demonstrate high rate of karyotype evolution. This rate is especially impressive in Agrodiaetus butterflies that rapidly evolved the greatest chromosome number diversity known in animal kingdom within a single subgenus. Here we analyzed karyotype evolution in Agrodiaetus using phylogenetic comparative methods. We found that chromosome numbers possess a strong phylogenetic signal. This disproves the chromosome megaevolution model that proposes multiple chromosome rearrangements to accumulate independently in each of closely related species. We found that Brownian motion gives a more adequate description of observed trait changes than Ornstein-Uhlenbeck model. This indicates that chromosome numbers evolve via random walk along branches of the phylogeny. We discovered a correlation between karyotype changes and phylogeny branch lengths. This gradual pattern is inconsistent with the hybrid-sterility model which, due to association of major chromosome changes with cladogenetic events, predicts a high degree of punctualism in karyotype evolution. Thus, low underdominace of chromosomal rearrangements and/or prevalence of the recombination-suppression model over the hybrid-sterility model of chromosome speciation are the most common engines of the runaway chromosome number change observed.

Karyotypes of some pest insects

Структура кариотипа у высших чешуекрылых (Lepidoptera, Papilionomorpha)

Citation: Vershinina AO, Anokhin BA, Lukhtanov VA (2015) Ribosomal DNA clusters and telomeric (TTAGG)n repeats in blue butterflies (Lepidoptera, Lycaenidae) with low and high chromosome numbers. Comparative Cytogenetics 9(2): 161–171. Abstract Ribosomal DNA clusters and telomeric repeats are important parts of eukaryotic genome. However, little is known about their organization and localization in karyotypes of organisms with holocentric chromosomes. Here we present first cytogenetic study of these molecular structures in seven blue butterflies of the genus Polyommatus Latreille, 1804 with low and high chromosome numbers (from n=10 to n=ca.108) using fluorescence in situ hybridization (FISH) with 18S rDNA and (TTAGG) n telomeric probes. FISH with the 18S rDNA probe showed the presence of two different variants of the location of major rDNA clusters in Polyommatus species: with one or two rDNA-carrying chromosomes in haploid karyotype. We discuss evolutionary trends and possible mechanisms of changes in the number of ribosomal clusters. We also demonstrate that Polyommatus species have the classical insect (TTAGG) n telomere organization. This chromosome end protection mechanism probably originated de novo in small chromosomes that evolved via fragmentations.