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Multiple Independent Evolutionary Losses of XY Pairing at Meiosis in the Grey Voles

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Multiple Independent Evolutionary Losses of XY Pairing at Meiosis in the Grey Voles Multiple independent evolutionary losses of XY pairing at meiosis in the grey voles Pavel M. Borodin, Ekaterina A. Basheva, Anna A. Torgasheva, Olesya A. Dashkevich, Fedor N. Golenishchev, Irina V. Kartavtseva, et al. Chromosome Research The Biology of Chromatin and Chromosomes ISSN 0967-3849 Volume 20 Number 2 Chromosome Res (2012) 20:259-268 DOI 10.1007/s10577-011-9261-0 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science+Business Media B.V.. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy Chromosome Res (2012) 20:259–268 DOI 10.1007/s10577-011-9261-0 Multiple independent evolutionary losses of XY pairing at meiosis in the grey voles Pavel M. Borodin & Ekaterina A. Basheva & Anna A. Torgasheva & Olesya A. Dashkevich & Fedor N. Golenishchev & Irina V. Kartavtseva & Kazuyuki Mekada & Beth L. Dumont Received: 5 October 2011 /Revised and Accepted: 23 November 2011 /Published online: 13 December 2011 # Springer Science+Business Media B.V. 2011 Abstract In many eutherian mammals, X–Ychromo- species. Our sample includes ten species of the tribe some pairing and recombination is required for meiotic Microtini and two species of the tribe Lagurini. This progression and correct sex chromosome disjunction. increased breadth of sampling allowed us to identify Arvicoline rodents present a notable exception to this asynaptic species in each major Microtine lineage. meiotic rule, with multiple species possessing asynaptic Evidently, the ability of the sex chromosomes to pair sex chromosomes. Most asynaptic vole species belong to and recombine in male meiosis has been independently the genus Microtus sensu lato. However, many of the lost at least three times during the evolution of Microtine species both inside and outside the genus Microtus dis- rodents. These results suggest a lack of evolutionary play normal X–Y synapsis at meiosis. These observa- constraint on X–Y synapsis in Microtini, hinting at the tions suggest that the synaptic condition was present in presence of alternative molecular mechanisms for sex the common ancestor of all voles, but gaps in current chromosome segregation in this large mammalian taxonomic sampling across the arvicoline phylogeny tribe. prevent identification of the lineage(s) along which the asynaptic state arose. In this study, we use electron and Keywords meiosis . recombination . synapsis . immunofluorescent microscopy to assess heterogametic synaptonemal complex . pseudoautosomal region . sex chromosome pairing in 12 additional arvicoline MLH1 . SCP3 . vole . Arvicolinae Responsible Editor: Herbert Macgregor. P. M. Borodin (*) : E. A. Basheva : A. A. Torgasheva : I. V. Kartavtseva O. A. Dashkevich Institute of Biology and Soil Science, Institute of Cytology and Genetics, Russian Academy of Sciences, Far Eastern Department, Russian Academy of Sciences, Siberian Department, Vladivostok 690022, Russia Novosibirsk 630090, Russia e-mail: [email protected] K. Mekada Experimental Animal Division, P. M. Borodin : O. A. Dashkevich RIKEN BioResource Center, Department of Cytology and Genetics, Tsukuba-shi, Ibaraki 305-0074, Japan Novosibirsk State University, Novosibirsk, Russia B. L. Dumont E. A. Basheva : F. N. Golenishchev Department of Genome Sciences, Zoological Institute, Russian Academy of Sciences, University of Washington, Sankt-Petersburg 199034, Russia Seattle, WA 98195-5065, USA Author's personal copy 260 P.M. Borodin et al. Abbreviations species with asynaptic sex chromosomes also pos- BSA Bovine serum albumin sess unusually large sex chromosomes that contain Cy3 Orange fluorescing cyanine large blocks of constitutive heterochromatin (Marchal et DAPI 4′-6-Diamidino-2-phenylindole al. 2004). Whether this unique karyotypic feature is EM Electron microscopy functionally related to sex chromosome behavior at FITC Fluorescein isothiocyanate meiosis remains to be elucidated. FM Fluorescent microscopy Arvicoline rodents present an especially powerful MLH1 Homolog of prokaryotic mutL 1 mismatch test case for studying X–Y pairing and recombination repair protein at meiosis. Arvicolinae is a speciose mammalian sub- SC Synaptonemal complex family in which many species with asynaptic sex chro- SCP3 Synaptonemal complex protein 3 mosomes have been found (Fig. 1). The availability of closely related species that follow distinct meiotic para- digms provides a unique model system for dissecting the molecular and evolutionary basis for the loss of sex Introduction chromosome pairing and recombination. Most of the voles with asynaptic sex chromosomes The segregation of homologous chromosomes into belong to the genus Microtus sensu lato. All species of daughter cells at meiosis depends on the timely and Palearctic subgenera Microtus, Agricola, Sumeriomys, precise execution of homolog pairing, synapsis, and Iberomys, Terricola, and Blanfordimys studied so far recombination. Unpaired chromosomes and chromo- are asynaptic (Ashley et al. 1989, 1990; Borodin et al. somes that fail to undergo recombination can activate 1995; Carnero et al. 1991; Jimenez et al. 1991;Rovatsos early meiotic checkpoints, leading to arrest of the et al. 2008;Wolfetal.1988). Normal X–Y synapsis has meiotic cell cycle or programmed cell death. Defects been observed in all studied species of East Asian sub- in meiotic chromosome pairing and recombination are genera Pallasiinus (Ashley and Fredga 1994;Borodinet established mechanisms of infertility in humans al. 1997, 1995;Mekadaetal.2001)andAlexandromys (Hassold and Hunt 2001). (Borodin et al. 2011). Synaptic sex chromosomes have Mammalian heterogametic sex chromosomes present also been found in arvicoline species closely related to a notable deviation from this meiotic routine. The X and the genus Microtus,suchasNeodon sikimensis (Mekada Y chromosomes are largely non-homologous, with only et al. 2002)andChionomys nivalis (Megias-Nogales et short terminal regions of sequence homology. Pairing al. 2003), and in the distantly related species Arvicola and recombination in these pseudoautosomal regions terrestris and Arvicola sapidus (Borodin et al. 1995; (PAR) is required for meiotic progression and proper Megias-Nogales et al. 2003), Ellobius talpinus disjunction of the sex chromosomes in many mammalian (Bogdanov et al. 1986), and six species of the genus species (Mangs and Morris 2007). Structural mutations Myodes (Ashley and Fredga 1994; Borodin et al. 1995; in the PAR have been directly linked to spermatogenic Iwasa et al. 1999). failure in humans and mice (Burgoyne et al. 1992; Together, these patterns suggest that the synaptic Mohandas et al. 1992), and divergence in the PAR condition is the ancestral state in arvicoline rodents. between isolated populations could provide an intrinsic Apparently, it has been retained in the East Asian genetic barrier to hybridization, driving the formation of lineage of the genus Microtus, but lost in the other new species. lineage (or lineages) of this genus (Borodin et al. 2011). Despite the clear link between X–Y pairing and However, the synaptic patterns of several lineages in the meiotic progression in many mammals, there are a genus Microtus sensu lato remain unknown. Determin- handful of exceptional species. For example, in ing the XY pairing status in Nearctic voles, which are marsupials and several rodent species, the X and Y considered a sister group to the Asian and Palearctic chromosomes remain unpaired throughout meiosis lineages (Conroy and Cook 2000), and in some early (Deakin et al. 2010). In these species, the sex branches of the tribe Microtini,suchasStenocranius chromosomes are sequestered into a dense sex and Lasiopodomys (Abramson et al. 2009), could help body, but they never synapse or recombine (Page shed light on the evolutionary origin(s) of XYasynapsis et al. 2006). Curiously, most of the mammalian on the arvicoline phylogeny. Author's personal copy Evolutionary losses of XY pairing in grey voles 261 Fig. 1 Informal supertree of the arvicoline rodents with a known pattern of X–Ypair- ing.Thetreeisbasedon published molecular phyloge- nies (Abramson et al. 2009; Bannikova et al. 2009, 2010; Conroy and Cook 2000; Jaarola et al. 2004). Nodes receiving less than moderate support are reduced to polyt- omies. Species names are given according to recent publications and the checklist (Wilson and Reeder 2005). The subgenus names are given in brackets; the names used in the original publica- tions are given in square brackets. Numbers in paren- theses indicate the source of information about X–Ysyn- aptic condition: 1 Ashley and Fredga 1994; 2 Borodin et al. 1995; 3 Iwasa et al. 1999; 4 Bogdanov et al. 1986; 5 Megias-Nogales et al. 2003; 6 Mekada et al. 2002; 7 Mekada et al. 2001; 8 Borodin et al. 1997; 9 Borodin et al. 2011; 10 Jimenez et al. 1991; 11 Ashley et al. 1990; 12 Wolf et al. 1988; 13 Ashley et al. 1989; 14 Rovatsos et al. 2008; 15 Carnero et al. 1991. Black lines indicate synaptic spe- cies; red lines, asynaptic Toward this goal, we applied electron and immuno- Our sample includes five species of the Nearctic grey fluorescent microscopy of surface-spread synaptonemal voles (Microtus
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