Insights into the karyotype and genome evolution of haplogyne spiders indicate a polyploid origin of lineage with holokinetic chromosomes

Abstract

Spiders are an ancient and extremely diverse animal order. They show a considerable diversity of genome sizes, karyotypes and sex chromosomes, which makes them promising models to analyse the evolution of these traits. Our study is focused on the evolution of the genome and chromosomes in haplogyne spiders with holokinetic chromosomes. Although holokinetic chromosomes in spiders were discovered a long time ago, information on their distribution and evolution in these arthropods is very limited. Here we show that holokinetic chromosomes are an autapomorphy of the superfamily Dysderoidea. According to our hypothesis, the karyotype of ancestral Dysderoidea comprised three autosome pairs and a single X chromosome. The subsequent evolution has frequently included inverted meiosis of the sex chromosome and an increase of 2 n . We demonstrate that caponiids, a sister clade to Dysderoidea, have enormous genomes and high diploid and sex chromosome numbers. This pattern suggests a polyploid event in the ancestors of caponiids. Holokinetic chromosomes could have arisen by subsequent multiple chromosome fusions and a considerable reduction of the genome size. We propose that spider sex chromosomes probably do not pose a major barrier to polyploidy due to specific mechanisms that promote the integration of sex chromosome copies into the genome.

Patterns of Sex Chromosome Differentiation in Spiders: Insights from Comparative Genomic Hybridisation

“…Some of these cases represent neo-sex chromosomes, which evolve by structural chromosome rearrangements between gonosomes and autosomes [18,21,[30][31][32][33][34][35]. Furthermore, the Y chromosome is involved in a peculiar X 1 X 2 Y system, which occurs in several families of haplogyne spiders [31,[36][37][38]. In all haplogynes described to date, the X 1 X 2 Y system is characterised by a specific structure and unusual achiasmatic pairing during male meiosis.…”

“…This system is usually formed by two large metacentric X chromosomes and a tiny metacentric Y microchromosome, which together form a trivalent by pairing via ends of their arms, without formation of chiasmata. The phylogenetic distribution of the X 1 X 2 Y system along with a conservative structure of these sex chromosomes suggest its considerable antiquity [31,37]. The origin of this system is unknown.…”

Cytogenetics of entelegyne spiders (Arachnida, Araneae) from southern Africa

“…Our cytogenetic results from southern African entelegynes fit with our knowledge of the general trends in karyotype diversification of the group. Compared to other ma-jor clades of spiders (Král et al 2006(Král et al , 2013(Král et al , 2019, Entelegynae karyotypes are more homogenous in 2n ranges and very conservative in morphology, which is nearly exclusively acrocentric (Araujo et al 2019, this study). The X 1 X 2 0 sex determination system is dominant in entelegynes.…”

“…This chromosome type is unique in spiders, and evolved only once in this order (e.g. Král et al 2006Král et al , 2019. The rest of haplogyne spiders typically possess a low number of biarmed chromosomes (2n♂ = 9-33, average 21) (Král et al 2006), with the exception of the presumably polyploid family Caponiidae (2n♂ = 55-152) (Král et al 2019).…”

“…Šťáhlavský et al 2006, 2012), our knowledge about spiders here is limited. A few attempts have been made to elucidate the karyotype diversity of mygalomorphs and haplogynes from this region (Král et al 2006(Král et al , 2013(Král et al , 2019. However, despite the enormous diversity of entelegynes, and our comparatively good knowledge about their cytogenetics worldwide, there is a significant lack of karyotype data from sub-Saharan Africa (Araujo et al 2019).…”