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

Abstract

Spiders are an intriguing model to analyse sex chromosome evolution because of their peculiar multiple X chromosome systems. Y chromosomes were considered rare in this group, arising after neo-sex chromosome formation by X chromosome-autosome rearrangements. However, recent findings suggest that Y chromosomes are more common in spiders than previously thought. Besides neo-sex chromosomes, they are also involved in the ancient X1X2Y system of haplogyne spiders, whose origin is unknown. Furthermore, spiders seem to exhibit obligatorily one or two pairs of cryptic homomorphic XY chromosomes (further cryptic sex chromosome pairs, CSCPs), which could represent the ancestral spider sex chromosomes. Here, we analyse the molecular differentiation of particular types of spider Y chromosomes in a representative set of ten species by comparative genomic hybridisation (CGH). We found a high Y chromosome differentiation in haplogyne species with X1X2Y system except for Loxosceles spp. CSCP chromosomes exhibited generally low differentiation. Possible mechanisms and factors behind the observed patterns are discussed. The presence of autosomal regions marked predominantly or exclusively with the male or female probe was also recorded. We attribute this pattern to intraspecific variability in the copy number and distribution of certain repetitive DNAs in spider genomes, pointing thus to the limits of CGH in this arachnid group. In addition, we confirmed nonrandom association of chromosomes belonging to particular CSCPs at spermatogonial mitosis and spermatocyte meiosis and their association with multiple Xs throughout meiosis. Taken together, our data suggest diverse evolutionary pathways of molecular differentiation in different types of spider Y chromosomes.

Identification of sex chromosomes using genomic and cytogenetic methods in a range-expanding spider, Argiope bruennichi (Araneae: Araneidae)

“…The pair associates at the centromeres with the multiple X chromosomes during male meiosis (Král, 2007). This pair has been termed "cryptic sex chromosome pair" (CSCP) (Sember et al, 2020) since the chromosomes are homomorphic (i.e., exhibit no morphological differentiation), and can only be detected under optimal conditions due to fragile meiotic association with the X chromosomes (Král, 2007;Král et al, 2011). Due to its discovery in some entelegyne lineages, as well as in more basally branching spider groups, it has been hypothesized that the CSCP represent ancestral spider sex chromosomes (Král, 2007;Král et al, 2011Král et al, , 2013Sember et al, 2020).…”

“…However, if it does exist in A. bruennichi, then the differentiation of X and Y must be very low, as we could not detect them with the given data, and thus the male Y sequences map to the X of the CSCP in the genome assembly. A very low differentiation between chromosomes X and Y of CSCP is supported by identical morphology of these chromosomes (Král, 2007;Král et al, 2011Král et al, , 2013, distribution of chiasmata, which can be formed along the entire or almost entire chromosome length, as well as by lack of differential hybridization between chromosomes of the CSCP, probed by comparative genomic hybridization (Sember et al, 2020).…”

“…The CSCP can only be detected under optimal conditions, as their meiotic association with the X chromosomes is fragile. Due to its discovery in some entelegyne lineages, as well as in more basally branching spider groups, it has been hypothesized that the CSCP represents ancestral spider sex chromosomes (Král, 2007; Král et al ., 2011, 2013; Sember et al ., 2020). Whether or not A. bruennichi possesses the CSCP is beyond the scope of this study.…”

Insights into the Karyotype Evolution of Charinidae, the Early-Diverging Clade of Whip Spiders (Arachnida: Amblypygi)

“…Given that mostly only males (in seven out of nine species) provided chromosome plates, one cannot exclude female heterogamety with morphologically differentiated sex chromosomes in whip spiders. Heteromorphic sex chromosomes occur in two tetrapulmonate groups, spiders [48,[67][68][69] and uropygids [70]. These orders exhibit male heterogamety.…”

Atypus karschiDönitz, 1887 (Araneae: Atypidae): an Asian purse-web spider established in Pennsylvania, USA

“…Most karyotype data on spiders concerns araneomorphs (42), but some karyotypes of mygalomorph spiders have been published (17,18,20,43,44). Representatives of the superfamily Atypoidea display a similar range of diploid numbers as araneomorph spiders (from 14 to 47).…”