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Genetica (2010) 138:1181–1189 DOI 10.1007/s10709-010-9509-1 Prevalence of B chromosomes in Orthoptera is associated with shape and number of A chromosomes Brian G. Palestis • Josefa Cabrero • Robert Trivers • Juan Pedro M. Camacho Received: 29 June 2010 / Accepted: 18 October 2010 / Published online: 31 October 2010 Ó Springer Science+Business Media B.V. 2010 Abstract We analyze the prevalence of B chromosomes Keywords B chromosome Á Centromeric drive Á in 1,601 species of orthopteran insects where chromosome Chromosome number Á Chromosome shape Á Insects Á number and shape are known. B chromosomes have been Orthoptera reported in 191 of these species. Bs are not uniformly distributed among orthopteran superfamilies, with evident hotspots in the Pyrgomorphoidea (32.3% of species car- Introduction rying Bs), Grylloidea (14.9%), Acridoidea (14.6%) and Tetrigoidea (14.3%). As expected under the theory of B chromosomes are additional dispensable chromosomes centromeric drive, we found a correlation between B which constitute one of the most widespread numerical chromosome presence and A chromosome shape—Bs are polymorphisms in many eukaryote species (reviewed in more frequent in karyotypes with more acrocentric A Camacho 2005; Burt and Trivers 2006). Many of them chromosomes. We also found that Bs are less common in show a selfish behaviour during transmission, thus gaining species with high chromosome numbers and appear to be a crucial advantage for invasion of new populations. This most common at the modal chromosome number property, named drive or accumulation, is also essential for (2n = 24). Study effort, measured for each genus, was not B chromosome maintenance in natural populations. In associated with B prevalence, A chromosome shape or A addition, many B chromosomes are associated with a fit- chromosome number. Our results thus provide support for ness decrease in the individuals carrying them, thus centromeric drive as an important and prevalent force in behaving as true parasites. These two properties, drive and the karyotypic evolution of Orthoptera, just as it appears to harmfulness, justify their consideration as genome para- be in mammals. We suggest that centromeric drive may sites (O¨ stergren 1945). Although most B chromosomes fit provide a mechanistic explanation for White’s principle of this parasitic model, where B frequency in natural popu- karyotypic orthoselection. lations may reach a stable equilibrium between drive and deleterious effects, there are also cases where Bs are fre- quent but lack apparent drive, some even showing a benefit for those individuals carrying them. This alternative model, B. G. Palestis the heterotic one, was first proposed by Darlington (1958) Department of Biological Sciences, Wagner College, and was supported by White (1973), who claimed that Bs Staten Island, NY, USA might prosper in the absence of drive, and their frequency might also reach equilibrium if they are beneficial at low J. Cabrero Á J. P. M. Camacho (&) Departamento de Gene´tica, Universidad de Granada, number but harmful at high numbers. In addition, parasitic 18071 Granada, Spain chromosomes may lose drive because of selection for e-mail: [email protected] resistance genes in the A chromosomes, thus becoming near-neutral elements. In this last case, B chromosome R. Trivers Department of Anthropology and Biological Science, frequency does not necessarily reach equilibrium but is Rutgers University, New Brunswick, NJ, USA constantly changing, with Bs passing through parasitic, 123 1182 Genetica (2010) 138:1181–1189 drive-suppressing and near-neutral stages (Camacho et al. In this report, we investigate whether chromosome 1997). In this kind of B, the near-neutral stage is much shape and number are associated with B chromosome longer than the other two and, during this time, it is even presence in the order Orthoptera, the insects with the possible for the appearance of a B-derived variant to highest number and frequency of Bs. The last compre- recover drive and become parasitic again (Zurita et al. hensive review of B chromosome occurrence in Orthoptera 1998). It is thus possible that many B chromosome systems was performed by Hewitt (1979), who reported B presence are long-lasting, as is also suggested by the 2 million year in 130 species. These last 31 years have been very inten- age calculated for maize B chromosomes (Lamb et al. sive in orthopteran cytogenetic research, and now this 2007) and the 750,000 years for Bs in Locusta migratoria figure is 210. Here we provide evidence that, in Orthoptera, (Teruel et al. 2010). Some B chromosome systems may chromosome shape and number are associated with B even survive speciation events (Camacho 2005). chromosome presence, in agreement with trends shown Previous analyses of B chromosome prevalence across previously in other organisms. species have shown that they are unequally spread over taxonomical groups, being particularly frequent in mono- cots (especially Commelinales and Liliales) among plants, Methods and orthopteran insects among animals (see Jones and Rees 1982; Camacho 2005; Levin et al. 2005). In looking for We built a spreadsheet database including cytogenetical reasons to explain the distribution of B chromosomes and taxonomical information on orthopteran species where across species, previous research has investigated the chromosome number and shape has been analysed. For this possible association between B chromosome presence and purpose, we first reviewed the 3,206 entries in a Reference factors such as breeding system, genome size, and A Manager database we had previously built with all reprints chromosome shape, number and ploidy (reviewed in collected for our 35 years of orthopteran chromosome Palestis et al. 2004b). In summary, these authors showed research. In addition, we reviewed the main cytogenetics that, in plants, (1) outbreeding favors harmful Bs whereas books including information on orthopteran chromosomes, beneficial Bs do best under inbreeding (Burt and Trivers such as Makino (1951), White (1973), Hewitt (1979) and 1998), (2) presence of B chromosomes is positively cor- Jones and Rees (1982). The taxonomical fields in our related with genome size (Trivers et al. 2004; Levin et al. spreadsheet database (suborder, superfamily, family, sub- 2005), and (3) B chromosomes are more likely in species family, tribe, genus and species) were established accord- with few A chromosomes (Trivers et al. 2004). In addition, ing to the Orthoptera Species File Online database Palestis et al. (2004a) showed that, in mammals, B chro- (http://orthoptera.speciesfile.org). The cytogenetic fields mosomes are more common in species with acrocentric were Bs (presence or absence), chromosome number in chromosomes, in agreement with expectations from the females (2n), number of chromosome arms in females theory of centromeric drive put forward by Pardo-Manuel (FN), proportion of one-armed chromosomes, and B de Villena and Sapienza (2001a, b). chromosome shape (number of arms in the B chromo- The theory of centromeric drive suggests the existence some). Information about genome size in orthopteran of a bias during female meiosis in the ability for capturing species was obtained from the Animal Genome Size centromeres by the oocyte and polar body poles, a bias that database (Gregory 2010: http://www.genomesize.com). frequently reverses in mammals so that most species either The major limitation to determining the factors that have mainly acrocentric or mainly metacentric chromo- make a species more likely to have B chromosomes is that somes (Pardo-Manuel de Villena and Sapienza 2001a, b). Bs, by definition, are not present in all individuals in a In species with karyotypes predominantly composed of species. Bs are therefore more likely to be observed in biarmed chromosomes, we can infer that Robertsonian well-studied species (Palestis et al. 2004b; Trivers et al. translocations have found an easy pathway to fixation, and 2004). For the Orthoptera it would be preferable to have a this could have taken place by a greater ability of the polar species-level index of study effort (e.g. number of pub- body to capture centromeres, thus capturing the two acro- lished cytogenetic papers for each species in the dataset), centrics in a trivalent of a heterozygous female, whereas but creating such an index for 1,601 species would be the metacentric would tend to go to the oocyte. In a species extremely labor-intensive and probably incomplete where the greater ability to capture centromeres is shown (Palestis et al. 2004b; Trivers et al. 2004). To create a by the oocyte, the predominant A chromosome shape substitute index of study effort, we calculated the propor- would be uni-armed and, since B chromosomes represent tion of species in a genus with known karyotypes. For this extra centromeres, they would also tend to go to the oocyte purpose, we compared the number of species of a given thus finding an easy way to drive and increase in frequency genus in our spreadsheet database with the total number of (Palestis et al. 2004a). species taxonomically described for that genus, as found in 123 Genetica (2010) 138:1181–1189 1183 the Orthoptera Species File Online database (http:// Results orthoptera.speciesfile.org). Species without published kar- yotypes are excluded from all other analyses to avoid Our first data collection included 210 orthopteran species creating a downward bias in estimates of B prevalence where B chromosome presence has been reported. How- across taxa (Palestis et al. 2004b). We also tested for ever, A chromosome shape was reported in only 191 of relationships between study effort and the predictor vari- these species, so that our subsequent analyses were limited ables to ensure no biases toward specific variables were to the database collection that included chromosome shape. present (Palestis et al. 2004b; Trivers et al. 2004). Unfor- Overall, 191 of 1,601 species (11.9%) with known karyo- tunately, within-genus study effort does not necessarily types are reported to have B chromosomes.

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