The role of chromosomal rearrangements and geographical barriers in the divergence of lineages in a South American subterranean rodent (Rodentia: Ctenomyidae: Ctenomys minutus)

Abstract

Identifying factors and the extent of their roles in the differentiation of populations is of great importance for understanding the evolutionary process in which a species is involved. Ctenomys minutus is a highly karyotype-polymorphic subterranean rodent, with diploid numbers ranging from 42 to 50 and autosomal arm numbers (ANs) ranging from 68 to 80, comprising a total of 45 karyotypes described so far. This species inhabits the southern Brazilian coastal plain, which has a complex geological history, with several potential geographical barriers acting on different time scales. We assessed the geographical genetic structure of C. minutus, examining 340 individuals over the entire distributional range and using information from chromosomal rearrangements, mitochondrial DNA (mtDNA) sequences and 14 microsatellite loci. The mtDNA results revealed seven main haplogroups, with the most recent common ancestors dating from the Pleistocene, whereas clustering methods defined 12 populations. Some boundaries of mtDNA haplogroups and population clusters can be associated with potential geographical barriers to gene flow. The isolation-by-distance pattern also has an important role in fine-scale genetic differentiation, which is strengthened by the narrowness of the coastal plain and by common features of subterranean rodents (that is, small fragmented populations and low dispersal rates), which limit gene flow among populations. A step-by-step mechanism of chromosomal evolution can be suggested for this species, mainly associated with the metapopulation structure, genetic drift and the geographical features of the southern Brazilian coastal plain. However, chromosomal variations have no or very little role in the diversification of C. minutus populations.

Figure 1

Sampling localities of Ctenomys minutus, and the distribution of the parental karyotypes and intraspecific hybrid zones. The seven mtDNA haplogroups are highlighted in the figure. BAR, Barco Beach; BJ1, Bujuru 1; BJ2, Bujuru 2; EBL, East Barros Lake; FOR, Fortaleza Lake; FSM, Farol de Santa Marta; GAI, Gaivota Beach; GUA, Guarita Beach; ILH, Ilhas; JG, Jaguaruna; MC, Morro dos Conventos; MOS, Mostardas; PAL, Palmares do Sul; PAS, Passinhos; PIT, Pitangueira; PST, Passo de Torres; OSO, Osório; 35, road km 35; 53, road km 53; 64, road km 64; 96, road km 96; 108, road km 108; 115, road km 115; SBL, South Barros Lake; 17S, 17 km south of Mostardas; 26S, 26 km south of Mostardas; SJN, São José do Norte; TRA, Tramandaí TV1, Tavares 1; TV2, Tavares 2.

Figure 2

Comparison of chromosomal rearrangements found among parental karyotypes based on the G-band patterns. The karyotype 2n=50a, AN=76 was used as standard to compare the chromosomal rearrangements in the other karyotypes. Squares highlight the main chromosomal rearrangements involved in the intraspecific hybrid zones. Modified from Freitas (1997), Gava and Freitas (2003) and Freygang et al. (2004).

Figure 3

(a) Bayesian phylogenetic tree; and (b) median-joining haplotype network topology obtained for concatenated mtDNA data. The seven main genetic haplogroups are highlighted by squares. Shading represents diploid numbers of parental karyotypes and intraspecific hybrids, as indicated in the legend. The abbreviations of the localities and the number of specimens per sampling site (within parentheses) are shown in the tree, and correspond to those in Table 1. The node posterior probabilities are given on the branches. Small black circles represent extinct or unsampled haplotypes in the network topology, and circle areas are proportional to the haplotype frequencies. *Diploid numbers of hybrids from crossing between 2n=42 × 48a; **diploid numbers of hybrids from crossing between 2n=42 × 46b. The color reproduction of this figure is available on the Hereditary journal online.

Figure 4

Bayesian skyline plots of concatenated mtDNA data for the seven main haplogroups of C. minutus: (a) North 1; (b) North 2; (c) Coast; (d) Barros Lake; (e) Mostardas; (f) Tavares; and (g) South. The gray area corresponds to the 95% highest posterior density limits for the effective population size. The thin and thick dotted lines are the lowest and the mean estimated tMRCA. Below the plot is the time represented in years, and in the left side are the effective population sizes.

Figure 5

Bayesian clustering and specimen assignments for the 12 clusters identified by the (a) Structure and (b) Tess programs. Each specimen is represented by a single bar, and each cluster by a color. Sampling sites are plotted geographically in the North–South direction, from left to right. Above plot: parental parapatric karyotypes, hybrid zones among them (HZ) and main possible geographical barriers. Below plot: BAR, Barco Beach; BJ1, Bujuru 1; BJ2, Bujuru 2; EBL, East Barros Lake; FOR, Fortaleza Lake; FSM, Farol de Santa Marta; GAI, Gaivota Beach; GUA, Guarita Beach; ILH, Ilhas; JG, Jaguaruna; MC, Morro dos Conventos; MOS, Mostardas; PAL, Palmares do Sul; PAS, Passinhos; PIT, Pitangueira; PST, Passo de Torres; OSO, Osório; 35, road km 35; 53, road km 53; 64, road km 64; 96, road km 96; 108, road km 108; 115, road km 115; SBL, South Barros Lake; 17S, 17 km south of Mostardas; 26S, 26 km south of Mostardas; SJN, São José do Norte; TRA, Tramandaí TV1, Tavares 1; TV2, Tavares 2. *Roman numbers correspond to Structure clusters, and the uppercase letters correspond to Tess clusters.