The evolution of a highly speciose group in a changing environment: are we witnessing speciation in the Iberá wetlands?

Abstract

Delimiting species is very conflicting in the case of very young taxa that are in the process of diversification, and even more difficult if the species inhabit a heterogeneous environment. In this case, even population delimitation is controversial. The South American genus of subterranean rodents Ctenomys is highly speciose, with 62 species that appeared in the lapse of 3 Myr. Within the genus, the 'perrensi' group, formed by three named species and a group of forms of unknown taxonomic status, inhabits the Iberá wetland, in northern Argentina. Almost every locality shows a particular chromosomal complement. To understand the relationships and the evolutionary process among species and populations, we examined mitochondrial DNA sequences and microsatellite genotypes. We found an isolation-by-distance pattern with evidence of cluster-like behaviour of the system. The mitochondrial DNA network revealed two different groups, separated by one of the main rivers of the region. Clustering methods delimited 12 different populations and five metapopulation lineages that seem to be evolving independently. We found evidence of ancient migration among localities at the centre of the distribution but no signals of current migration among the 12 delimited clusters. Some of the genetic clusters found included localities with different chromosomal numbers, which points to the existence of gene flow despite chromosomal variation. The evolutionary future of these five lineages is controlled by the dynamics of their habitat: if stable, they may become distinct species; otherwise, they may collapse into a hybrid swarm, forming a single evolving metapopulation.

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

“…The sharp increase in genetic and geographic distance correlations, until it reaches an irregular pattern, is expected under a model of isolation with asymmetric gene flow in a metapopulation. A similar pattern was observed in the perrensi group of ctenomyids (Fernández et al, 2012).…”

“…Studies by Freitas (2002, 2003), using cytogenetic data for the C. minutus hybrid zones between 2n ¼ 46a  48a and 2n ¼ 48a  42 showed no evidence of underdominance, and demonstrated that the chromosomal polymorphisms fail to cause sterility in heterotypes. The chromosomal rearrangements in the 'perrensi' group were considered to be the result of an ongoing isolation with a migration process, rather than representing a barrier to gene flow (Caraballo et al, 2012;Fernández et al, 2012). Some highly chromosomally polymorphic mammals, such as Mus musculus domesticus and Sorex araneus, show a step-bystep mechanism of karyotype evolution, similar to that of C. minutus.…”

“…The first hypothesis relies on the metapopulation structure, with small subpopulations distributed in patches of suitable habitats (Fernández et al, 2012). Whether a new chromosomal rearrangement causes little or no negative meiotic effects, it can be more easily fixed in peripheral and/or small isolated populations (Baker and Bickham, 1986) by means of genetic drift, spreading to new, recently colonized areas.…”

Integrative lineage delimitation in rodents of the Ctenomys Corrientes group

“…Sequences from the Entrerrianan populations of San Joaquín de Miraflores and Paso Vera do not belong to the Corrientes group, but instead fall into its sister clade, together with the also Entrerrianan population of Médanos and the Uruguayan Ctenomys pearsoni complex. In turn, the sequence from Costa Mansión, Ctenomys roigi topotype, forms a monophyletic group with the ones from Estancia San Luis, in agreement with chromosomal (Caraballo et al 2015) and SSR analyses (Gómez Fernández et al 2012). …”

“…Morphological analyses (Contreras and Scolaro 1986, Contreras 1988, Ortells 1990), cytogenetic studies , García et al 2000b, Argüelles et al 2001, Caraballo et al 2015, chromosome banding (Ortells 1995), satellite DNA dynamics (Caraballo et al 2010), allozymic distances (Ortells and Barrantes 1994), population genetic studies (Mirol et al 2010, Gómez Fernández et al 2012, and mitochondrial phylogenies (Giménez et al 2002, Caraballo et al 2012) have been performed. From a morphological perspective, the populations comprising the Corrientes group, even the ones considered to belong to different nominal species showed little or no differentiation (Figure 1, Ortells 1990) and hence are likely to be cryptic ones.…”