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Karyotype, sex determination, and meiotic chromosome behavior in two pholcid (Araneomorphae, Pholcidae) spiders: implications for karyotype evolution.

ABSTRACT: There are 1,111 species of pholcid spiders, of which less than 2% have published karyotypes. Our aim in this study was to determine the karyotypes and sex determination mechanisms of two species of pholcids: Physocyclus mexicanus (Banks, 1898) and Holocnemus pluchei (Scopoli, 1763), and to observe sex chromosome behavior during meiosis. We constructed karyotypes for P. mexicanus and H. pluchei using information from both living and fixed cells. We found that P. mexicanus has a chromosome number of 2n?=?15 in males and 2n?=?16 in females with X0-XX sex determination, like other members of the genus Physocyclus. H. pluchei has a chromosome number of 2n?=?28 in males and 2n?=?28 in females with XY-XX sex determination, which is substantially different from its closest relatives. These data contribute to our knowledge of the evolution of this large and geographically ubiquitous family, and are the first evidence of XY-XX sex determination in pholcids.

SUBMITTER: Golding AE

PROVIDER: S-EPMC3170389 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Karyotype, sex determination, and meiotic chromosome behavior in two pholcid (Araneomorphae, Pholcidae) spiders: implications for karyotype evolution.

Golding Adriana E AE Paliulis Leocadia V LV

PloS one 20110909 9

There are 1,111 species of pholcid spiders, of which less than 2% have published karyotypes. Our aim in this study was to determine the karyotypes and sex determination mechanisms of two species of pholcids: Physocyclus mexicanus (Banks, 1898) and Holocnemus pluchei (Scopoli, 1763), and to observe sex chromosome behavior during meiosis. We constructed karyotypes for P. mexicanus and H. pluchei using information from both living and fixed cells. We found that P. mexicanus has a chromosome number ...[more]

PMID: 21931842

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Project description:BackgroundDespite progress in genomic analysis of spiders, their chromosome evolution is not satisfactorily understood. Most information on spider chromosomes concerns the most diversified clade, entelegyne araneomorphs. Other clades are far less studied. Our study focused on haplogyne araneomorphs, which are remarkable for their unusual sex chromosome systems and for the co-evolution of sex chromosomes and nucleolus organizer regions (NORs); some haplogynes exhibit holokinetic chromosomes. To trace the karyotype evolution of haplogynes on the family level, we analysed the number and morphology of chromosomes, sex chromosomes, NORs, and meiosis in pholcids, which are among the most diverse haplogyne families. The evolution of spider NORs is largely unknown.ResultsOur study is based on an extensive set of species representing all major pholcid clades. Pholcids exhibit a low 2n and predominance of biarmed chromosomes, which are typical haplogyne features. Sex chromosomes and NOR patterns of pholcids are diversified. We revealed six sex chromosome systems in pholcids (X0, XY, X1X20, X1X2X30, X1X2Y, and X1X2X3X4Y). The number of NOR loci ranges from one to nine. In some clades, NORs are also found on sex chromosomes.ConclusionsThe evolution of cytogenetic characters was largely derived from character mapping on a recently published molecular phylogeny of the family. Based on an extensive set of species and mapping of their characters, numerous conclusions regarding the karyotype evolution of pholcids and spiders can be drawn. Our results suggest frequent autosome-autosome and autosome-sex chromosome rearrangements during pholcid evolution. Such events have previously been attributed to the reproductive isolation of species. The peculiar X1X2Y system is probably ancestral for haplogynes. Chromosomes of the X1X2Y system differ considerably in their pattern of evolution. In some pholcid clades, the X1X2Y system has transformed into the X1X20 or XY systems, and subsequently into the X0 system. The X1X2X30 system of Smeringopus pallidus probably arose from the X1X20 system by an X chromosome fission. The X1X2X3X4Y system of Kambiwa probably evolved from the X1X2Y system by integration of a chromosome pair. Nucleolus organizer regions have frequently expanded on sex chromosomes, most probably by ectopic recombination. Our data suggest the involvement of sex chromosome-linked NORs in achiasmatic pairing.

Project description:BackgroundPholcidae represent one of the largest and most diverse spider families and have been subject to various studies regarding behavior and reproductive biology. In contrast to the solid knowledge on phylogeny and general reproductive morphology, the primary male reproductive system is strongly understudied, as it has been addressed only for few species. Those studies however suggested a high diversity of sperm and seminal secretions across the family. To address this disparity and reconstruct the evolution of sperm traits, we investigate the primary male reproductive system of pholcid spiders by means of light, X-ray, and transmission electron microscopy using a comprehensive taxon sampling with 46 species from 33 genera, representing all five subfamilies.ResultsOur data show a high disparity of sperm morphology and seminal secretions within pholcids. We document several sperm characters that are unique for pholcids, such as a helical band (Pholcinae) or a lamellate posterior centriolar adjunct material (Modisiminae). Character mapping revealed several putative synapomorphies for individual taxa. With regard to sperm transfer forms, we found that synspermia occur only in the subfamily Ninetinae, whereas the other subfamilies have cleistospermia. In several species with cleistospermia, we demonstrate that spermatids remain fused until late stages of spermiogenesis before ultimately separating shortly before the coiling process. Additionally, we explored the previously hypothesized correlation between sperm size and minimum diameter of the spermophor in the male palpal organ. We show that synspermia differ strongly in size whereas cleistospermia are rather uniform, but neither transfer form is positively correlated with the diameter of the spermophor.ConclusionsOur data revealed a dynamic evolution of sperm characters, with convergences across all subfamilies and a high level of homoplasy. The present diversity can be related to subfamily level and allows for assignments of specific subtypes of spermatozoa. Our observations support the idea that Ninetinae are an ancestral clade within Pholcidae that have retained synspermia and that synspermia represent the ancestral sperm transfer form of Pholcidae.

Project description:With almost 600 species, the latest molecular phylogeny of pholcid spiders (Eberle et al. 2018, BMC Evolutionary Biology) more than triples the largest previously available molecular phylogeny of the family. At the level of genera, the coverage is high (86%, i.e., 75 of the 87 named genera), and at the level of subfamilies it is complete. The present paper is an effort to critically evaluate the implications of this phylogeny for pholcid systematics. The analyses largely support the division of Pholcidae into five subfamilies: Ninetinae, Arteminae, Modisiminae, Smeringopinae, and Pholcinae. Their compositions are largely unchanged except that Chisosa Huber, 2000 is moved from Ninetinae to Arteminae. The positions of Artema Walckenaer, 1837 and Priscula Simon, 1893 in this system remain dubious. Relationships among subfamilies remain weakly supported, except for the sister group relationship between Smeringopinae and Pholcinae. Several major clades within subfamilies are separated from each other along geographical boundaries; for example within Modisiminae a South American clade and a Central + North American + Caribbean clade, and within Smeringopinae a Sub-Saharan clade and a clade ranging from the Mediterranean to Central Asia. Central + North American + Caribbean clades in both Ninetinae and Modisiminae may originate from South American ancestors. Many taxonomic changes are suggested by the data, some of which are formally implemented herein. Two new genera result from the splitting of Calapnita Simon, 1892 and Panjange Deeleman-Reinhold & Deeleman, 1983, respectively: Nipisa Huber, gen. n.; and Apokayana Huber, gen. n. Nine new genera result from splitting of Pholcus: Cantikus Huber, gen. n.; Kelabita Huber, gen. n.; Kintaqa Huber, gen. n.; Muruta Huber, gen. n.; Meraha Huber, gen. n.; Paiwana Huber, gen. n.; Pribumia Huber, gen. n.; Teranga Huber, gen. n.; and Tissahamia Huber, gen. n. Two genera are newly synonymized: Platnicknia Özdikmen & Demir, 2009 is synonymized with Modisimus Simon, 1893; Sihala Huber, 2011 is synonymized with Pholcus Walckenaer, 1805. Pholcusagadir Huber, 2011 is moved to Micropholcus Deeleman-Reinhold & Prinsen, 1987, resulting in the new combination Micropholcusagadir (Huber, 2011).

Dataset Information

Karyotype, sex determination, and meiotic chromosome behavior in two pholcid (Araneomorphae, Pholcidae) spiders: implications for karyotype evolution.

Publications

Karyotype, sex determination, and meiotic chromosome behavior in two pholcid (Araneomorphae, Pholcidae) spiders: implications for karyotype evolution.

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