Integration of molecular cytogenetics, dated molecular phylogeny, and model-based predictions to understand the extreme chromosome reorganization in the Neotropical genus Tonatia (Chiroptera: Phyllostomidae)

Abstract

BackgroundDefining factors that contributed to the fixation of a high number of underdominant chromosomal rearrangements is a complex task because not only molecular mechanisms must be considered, but also the uniqueness of natural history attributes of each taxon. Ideally, detailed investigation of the chromosome architecture of an organism and related groups, placed within a phylogenetic context, is required. We used multiple approaches to investigate the dynamics of chromosomal evolution in lineages of bats with considerable karyotypic variation, focusing on the different facets contributing to fixation of the exceptional chromosomal changes in Tonatia saurophila. Integration of empirical data with proposed models of chromosome evolution was performed to understand the probable conditions for Tonatia’s karyotypic evolution.ResultsThe trajectory of reorganization of chromosome blocks since the common ancestor of Glossophaginae and Phyllostominae subfamilies suggests that multiple tandem fusions, as well as disruption and fusions of conserved phyllostomid chromosomes were major drivers of karyotypic reshuffling in Tonatia. Considerable variation in the rates of chromosomal evolution between phyllostomid lineages was observed. Thirty–nine unique fusions and fission events reached fixation in Tonatia over a short period of time, followed by ~12 million years of chromosomal stasis. Physical mapping of repetitive DNA revealed an unusual accumulation of LINE-1 sequences on centromeric regions, probably associated with the chromosomal dynamics of this genus.ConclusionsMultiple rearrangements have reached fixation in a wave-like fashion in phyllostomid bats. Different biological features of Tonatia support distinct models of rearrangement fixation, and it is unlikely that the fixations were a result of solely stochastic processes in small ancient populations. Increased recombination rates were probably facilitated by expansion of repetitive DNA, reinforced by aspects of taxon reproduction and ecology.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0494-y) contains supplementary material, which is available to authorized users.

Centromeric enrichment of LINE-1 retrotransposons and its significance for the chromosome evolution of Phyllostomid bats

“…Examples include gibbons and macropodid marsupials, which, interestingly, have experienced rapid chromosomal evolution together with centromeric enrichment of retroelements (Bulazel et al 2007;Wichman et al 1991). In the case of phyllostomid bats, all analyzed species present highly derived karyotypes from the proposed 2n = 46 ancestral condition for the family, and all but C. perspicillata show centromere signal using LINE-1 probes (see also Sotero-Caio et al 2015).…”

Chromosomal Evolution in Chiroptera

“…The family Phyllostomidae is the only bat group, for which LINE-1 chromosomal distribution has been investigated, also revealing patterns with important implications in a chromosome evolution perspective. In these bats, differential accumulation patterns are found among species [ 40 , 41 , 42 ], and a massive centromere enrichment of these sequences has been proposed as one of the factors contributing to the genome plasticity of Phyllostomidae in terms of chromosome rearrangements, especially Robertsonian translocations [ 43 ].…”

“…The distribution of telomeric sequences, on the other hand, does not seem as restricted as rDNA or correlated with small genome size in bats. For example, many species present massive amounts of the TTAGGG(n) in pericentromeric regions [ 41 , 44 , 51 ]. In these cases, it is hypothesized that amplification of telomeric sequences is directly linked with the expansion of satellite families that have incorporated the canonical telomere sequence [ 52 ].…”

Repetitive DNA profiles Reveal Evidence of Rapid Genome Evolution and Reflect Species Boundaries in Ground Beetles

“…These mobilized fragments of rDNA can be thought of newly birthed, rDNA-like repetitive elements. Mobilization of rDNA has been documented using cytogenetic methods in many groups including plants (Raskina et al 2004;Qi et al 2015;Ding et al 2016;Wang et al 2016), fish (Martins et al 2006;Da Silva et al 2012;Symonová et al 2013Symonová et al , 2017, protists (Gong et al 2013), insects (Cabral-de-Mello et al 2010, 2011Nguyen et al 2010;Panzera et al 2012;Palacios-Gimenez and Cabral-de-Mello 2015), bivalves (Pérez-García et al 2014), and mammals (Sotero-Caio et al 2015), and is regarded as strong evidence of rapid rearrangements over short time scales (Jiang and Gill 1994;Raskina et al 2004Raskina et al , 2008. Mobilization of such multicopy gene families into heterochromatic regions is thought to be mediated through processes such as retrotransposon activity (Dimitri et al 1997;Dimitri and Junakovic 1999;Symonová et al 2013;de Bello Cioffi et al 2015) and ectopic recombination (Nguyen et al 2010).…”