Preferential segregation of metacentric chromosomes in simple Robertsonian heterozygotes of Sorex araneus

Abstract

One of the hypotheses explaining preferential transmission of metacentrics among simple Robertsonian (Rb) heterozygotes of the common shrew (Sorex araneus L.) invokes the existence of meiotic drive. Thus far, evidence that metacentrics are favoured at meiosis has been obtained indirectly, on the basis of crosses made under controlled conditions. The aim of the present work was to test the hypothesis in a direct study. We analysed products of chromosome segregation among 12 simple heterozygote male subjects from a wild population, with regard to jl, io, nr and mn Rb fusions. We were able to demonstrate significant segregation distortion in favour of all four metacentrics. The level of preferential segregation was independent either of the composition of chromosome arms or the dimensions of metacentrics. We also found that X chromosomes were favoured over Y1Y2 chromosomes during segregation. We discuss the role of meiotic drive in the evolutionary success of metacentric chromosomes in S. araneus, as well as in the emergence of post-hybridization modifications in the zones of contact between races.

Extensive Robertsonian polymorphism in the African rodentGerbillus nigeriae: geographic aspects and meiotic data

“…Fedyk & Chetnicki, 2007), with similar values sometimes observed between simple and complex Rb heterozygous animals (e.g. Fedyk & Chetnicki, 2007, 2010).…”

“…In the common shrew Sorex araneus , another well‐studied species, meiotic non‐disjunction rates in males were found to be very variable between individuals (e.g. Fedyk & Chetnicki, 2007), with similar values sometimes observed between simple and complex Rb heterozygous animals (e.g. Fedyk & Chetnicki, 2007, 2010).…”

“…S. araneus provides some rare cases of true polymorphisms (i.e. that are not associated with hybrid zones; see for instance: Polyakov et al , 1997; Searle & Wojcik, 1998;Szalaj et al , 1999; Fedyk & Chetnicki, 2007; quoted by Banaszek et al , 2009). Only very rare meiotic analyses have been performed on individuals from these particular populations, and have shown that no‐disjunction rates in simple Rb heterozygotes ranged between 1.2 and 7.4% (see table 3 in Fedyk & Chetnicki, 2007).…”

Chromosomal polymorphism in mammals: an evolutionary perspective

“…In the latter, Rb heterozygosity was stable through time (∼20 generations) and not associated with a decrease in the fertility of this rodent species (Nachman & Myers, ; Nachman, ). In common shrews, Sorex araneus , non‐disjunction rates in simple heterozygotes varied between 1.2 and 7.4% (Table 3 in Fedyk & Chetnicki, ), whereas in house mice, germ cell death values ranged from 19.5% in standard individuals to 30.2% in single Rb heterozygotes (Sans‐Fuentes et al ., ). Similarly, a 3–5% decrease in fertility in cattle was noted for Rb (1;29) and unbalanced gametes may be as frequent as 4.1% in cows and 2.8% in bulls (Bonnet‐Garnier et al ., ).…”

“…Holochilus brasiliensis : Nachman, ; Mus spp. : Castiglia & Capanna, ; de Villena & Sapienza, ; Sorex araneus : Wyttenbach, Borodin & Hausser, ; Fedyk & Chetnicki, ; humans: de Villena & Sapienza, ; see also King, for a short review on the blue fox, Alopex lagopus ). The chromosome that is favoured depends on the species‐specific karyotypic background: acrocentrics are favoured over metacentrics in acrocentric‐rich karyotypes such as those of shrews and marsh rats (Nachman, ) as well as the house mouse (de Villena & Sapienza, ), while the opposite pattern is observed in the metacentric‐rich human karyotype (de Villena & Sapienza, ).…”