Simultaneous Mendelian and clonal genome transmission in a sexually reproducing, all-triploid vertebrate

Abstract

Meiosis in triploids faces the seemingly insuperable difficulty of dividing an odd number of chromosome sets by two. Triploid vertebrates usually circumvent this problem through either asexuality or some forms of hybridogenesis, including meiotic hybridogenesis that involve a reproductive community of different ploidy levels and genome composition. Batura toads (Bufo baturae; 3n ¼ 33 chromosomes), however, present an all-triploid sexual reproduction. This hybrid species has two genome copies carrying a nucleolus-organizing region (NORþ) on chromosome 6, and a third copy without it (NOR2). Males only produce haploid NORþ sperm, while ova are diploid, containing one NORþ and one NOR2 set. Here, we conduct sibship analyses with co-dominant microsatellite markers so as (i) to confirm the purely clonal and maternal transmission of the NOR2 set, and (ii) to demonstrate Mendelian segregation and recombination of the NORþ sets in both sexes. This new reproductive mode in vertebrates ('pre-equalizing hybrid meiosis') offers an ideal opportunity to study the evolution of non-recombining genomes. Elucidating the mechanisms that allow simultaneous transmission of two genomes, one of Mendelian, the other of clonal inheritance, might shed light on the general processes that regulate meiosis in vertebrates.

High male incidence and evolutionary implications of triploid form in northeast Asia Carassius auratus complex

“…However, most of unisexual vertebrates, such as kleptogenetic Ambystoma salamanders (Bi and Bogart, 2010;Spolsky et al, 1992), hybridogenetic Poeciliopsis fish (Quattro et al, 1992), gynogenetic Amazon molly (Lampert and Schartl, 2008;Schartl et al, 1995), Phoxinus eosneogaeus hybrids (Angers and Schlosser, 2007), and gynogenetic Cobitis (Janko et al, 2003), have been revealed to have long history and large ranges of geographical distribution (Avise, 2008). And, high genetic diversity has been extensively observed in gynogenetic or hybridogenetic fish (Angers and Schlosser, 2007;Cunha et al, 2011;Schmidt et al, 2011;Stöck et al, 2012), kleptogenetic amphibians (Bi and Bogart, 2010) and parthenogenetic reptiles (Fujita et al, 2007;Kupriyanova, 2009). Significantly, these rare unisexual animals are largely associated with polyploidy origin (Neaves and Baumann, 2011;Otto et al, 2007).…”

“…In the past decade, a lot of genetic knowledge including molecular basis of reproduction trait and numerous polymorphic DNA markers has been investigated and characterized from the triploid form (Gui and Zhou, 2010;Gui and Zhu, 2012). Similar to other polyploid salamanders, frogs and fish (Lampert and Schartl, 2010;Schlupp, 2005;Stöck et al, 2012), the triploid form can also reproduce by sperm-dependent gynogenesis, and many diverse gynogenetic clones have been discriminated by different genetic markers, such as transferrin Yang et al, 2001, RAPD and SCAR markers (Zhou et al, 2001(Zhou et al, , 2000b, microsatellite (Guo and Gui, 2008) and mtDNA sequence (Apalikova et al, 2008;Brykov et al, 2005;Li and Gui, 2008). Interestingly, a minor but significant portion (approx 1-10%) of triploid males were found in the triploid form, and normal sperm production and their sexual reproduction ability have been demonstrated by experimental propagation and genetic analysis in the triploid form (Gui and Zhou, 2010;Peng et al, 2009;Sun et al, 2010;Zhou et al, 2000a).…”

Origin and genome evolution of polyploid green toads in Central Asia: evidence from microsatellite markers

“…We also confirmed with nuclear markers that the maternal ancestor (B m ) of B. baturae was related to B. shaartusiensis. These new data represent the first nuclear and multilocus evidence for the maternal ancestry of B. baturae, which is one of the few gonochoristic all-triploid vertebrates (Stöck et al, 2012), for which previous hints on this hybrid species' maternal ancestor came only from mtDNA (Litvinchuk et al, 2011). The close relationship between B. baturae and B. shaartusiensis, that had been inferred from identical mtDNA sequences (Litvinchuk et al, 2011; Figure 1), contrasts with the deeper Stöck et al 2012) Bp1 Bp1 (= NOR+ in Stöck et al 2012) Bm Bp2 Bp2 (=NOR+ in Stöck et al 2012) Pm Pm (=TT in Stöck et al 2010) Pp Pp (=LL in Stöck et al 2010) …”

“…The ancestor of the two paternal sets (B p B p ) also remains unidentified (Figure 1). Triploidy is maintained by differential male and female forms of meioses: in the male germ line, the B m set (referred to as NOR-in Stöck et al, 2012) is eliminated, followed by a diploid meiosis of the B p sets (referred to as NOR+ in Stöck et al, 2012) that only produces recombined haploid B p sperm, whereas in the female germ line, the B m set is first duplicated, followed by a tetraploid meiosis that produces diploid B m B p ovules (Stöck et al, 2012). Hence, the B p set is sexually transmitted by both sexes, whereas the B m set is only maternally and clonally transmitted, along with mtDNA.…”

“…Hence, the B p set is sexually transmitted by both sexes, whereas the B m set is only maternally and clonally transmitted, along with mtDNA. This unique mode of transmission (termed 'pre-equalizing hybrid meiosis' by Stöck et al, 2012) is expected to bear important consequences on the evolution of the B m set, by strongly enhancing genetic drift and drastically reducing the efficiency of selection. The effective population size of the B m set is reduced to one quarter that of the B p sets, and the absence of recombination over large genomic regions is expected to induce strong Hill-Robertson interferences between co-segregating loci (e.g., McVean and Charlesworth, 2000): deleterious mutations can get fixed by hitchhiking with beneficial ones during selective sweeps or, conversely, beneficial alleles can be eliminated by selection against co-segregating deleterious mutations (background selection; Charlesworth, 1994).…”