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

Cibele G Sotero-Caio,Marianne Volleth,Robert J Baker,Federico G Hoffmann,Luann Scott,Holly A Wichman,Fengtang Yang

doi:10.1186/s12862-015-0494-y

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.

Highlights

Defining factors that contributed to the fixation of a high number of underdominant chromosomal rearrangements is a complex task because molecular mechanisms must be considered, and the uniqueness of natural history attributes of each taxon
The syntenies of most Macrotus californicus (MCA) chromosomes appeared disrupted on the Tonatia saurophila (TSA) karyotype, except for seven chromosome pairs, which seemed to have fused to other chromosomes as entire syntenic blocks (MCA 9, 11, 14, 15, 17, 18, and 19)
Extensive and conservative chromosomal evolution in Phyllostominae and Glossophaginae Our results show that the rates of chromosomal evolution since the divergence of the lineages that gave rise to the analyzed species were not constant over time, and that the set of rearrangements leading to the chromosomal constitution of genera such as Tonatia (Phyllostominae) and Anoura (Glossophaginae), have occurred as the result of waves of rearrangements specific to those lineages

Summary

Introduction

Defining factors that contributed to the fixation of a high number of underdominant chromosomal rearrangements is a complex task because molecular mechanisms must be considered, and the uniqueness of natural history attributes of each taxon. How chromosomal rearrangements become established in natural populations has been a recurrent question in evolutionary cytogenetics for decades [1,2,3]. The absence of “the one model” of chromosomal fixation can be attributed to the amount of variables associated with cellular, molecular, ecological, and population distinctiveness of each taxonomic group where chromosome rearrangements have become established [4]. The widespread model predicts that chromosome rearrangements resulting in underdominance require small population sizes to achieve fixation [1, 5]. It is noteworthy that some models of chromosomal speciation intrinsically bear assumptions applicable to models of rearrangement fixation within a population (see [7] for a review)

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