Enrique P. Lessa

Genetic footprints of demographic expansion in North America, but not Amazonia, during the Late Quaternary

The biotic consequences of climate change have attracted considerable attention. In particular, the “refugial debate” centers on the possible retraction of habitats to limited areas that may have served as refuges for many associated species, especially during glaciations of the Quaternary. One prediction of such scenarios is that populations must have experienced substantial growth accompanying climatic amelioration and the occupation of newly expanded habitats. We used coalescence theory to examine the genetic evidence, or lack thereof, for late Pleistocene refugia of boreal North American and tropical Amazonian mammals. We found substantial and concordant evidence of demographic expansion in North American mammals, particularly at higher latitudes. In contrast, small mammals from western Amazonia appear to have experienced limited or no demographic expansion after the Late Pleistocene. Thus, demographic responses to climate change can be tracked genetically and appear to vary substantially across the latitudinal gradient of biotic diversity.

Screening techniques for detecting allelic variation in DNA sequences

This article reviews four ‘DNA screening techniques’, namely heteroduplex analysis, single‐strand conformational polymorphism (SSCP), denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) as tools for the study of allelic variation in natural populations. The resolving power, advantages, and limitations of each technique are discussed and compared. We also provide some criteria for choosing among techniques and illustrate some practical issues with examples taken primarily from our own laboratory experience.

Genetic footprints of late Quaternary climate change in the diversity of Patagonian‐Fueguian rodents

Species are impacted by climate change at both ecological and evolutionary time scales. Studies in northern continents have provided abundant evidence of dramatic shifts in distributions of species subsequent to the last glacial maximum (LGM), particularly at high latitudes. However, little is known about the history of southern continents, especially at high latitudes. South America is the only continent, other than Antarctica, that extends beyond 40 degrees S. Genetic studies of a few Patagonian species have provided seemingly conflicting results, indicating either postglacial colonization from restricted glacial refugia or persistence through glacial cycles and in situ differentiation. Using mitochondrial DNA sequences of 14 species of sigmodontine rodents, a major faunal ensemble of Patagonia and Tierra del Fuego, we show that at least nine of these species bear genetic footprints of demographic expansion from single restricted sources. However, timing of demographic expansion precedes the LGM in most of these species. Four species are fragmented phylogeographically within the region. Our results indicate that (i) demographic instability in response to historical climate change has been widespread in the Patagonian-Fueguian region, and is generally more pronounced at high latitudes in both southern and northern continents; (ii) colonization from lower latitudes is an important component of current Patagonian-Fueguian diversity; but (iii) in situ differentiation has also contributed to species diversity.

Genetic and geographic differentiation in the rio negro tuco-tuco (Ctenomys rionegrensis): Inferring the roles of migration and drift from multiple genetic markers

Abstract Among tuco‐tucos, Ctenomys rionegrensis is especially amenable to the study of the forces driving population differentiation because of the restricted geographic range it occupies in Uruguay. Within this limited area, the Rio Negro tuco‐tuco is limited to sandy soils. It nonetheless exhibits remarkable variation in pelage color, including melanic, agouti, and dark‐backed individuals. Two hypotheses have been put forth to explain this pattern: (1) local differentiation and fixation of alternative pelage types by genetic drift under limited gene flow; or (2) fixation by natural selection that may take place even in the presence of gene flow. A previous allozyme study rejected the genetic drift hypothesis on the basis of high inferred levels of migration. New estimates of gene flow from microsatellites and mitochondrial cytochrome b sequences were obtained for C. rionegrensis populations to further test these hypotheses. Much lower levels of gene flow were estimated with these more sensitive markers. Microsatellite‐based estimates of gene flow are close to zero and may come closest to estimating current levels of migration. A lack of equilibrium between migration and genetic drift is also strongly suggested by the absence of an isolation‐by‐distance pattern found in all three genetic datasets. The microsatellite genotype data show that the species is strongly structured geographically, with subpopulations constituting distinct genetic entities. If current levels of gene flow are very low, as indicated by the new data, the local fixation of alternative alleles, including those responsible for pelage color polymorphism, is possible by drift alone. A scenario is thus proposed in which the species expanded in the recent past from a more restricted geographic range and has subsequently differentiated in near isolation, with genetic drift possibly playing a primary role in overall genetic differentiation. The local fixation of pelage color types could also be due to drift, but selection on this trait cannot be ruled out without direct analysis.

Rapid Diversification of South American Tuco-Tucos (Ctenomys; Rodentia, Ctenomyidae): Contrasting Mitochondrial and Nuclear Intron Sequences

Abstract Subterranean tuco-tucos (genus Ctenomys) are a speciose group of South American hystricognath rodents, often taken as an example of explosive speciation. The 4th intron of the rhodopsin gene (567 bp) and partial sequence of the 2nd intron of the vimentin gene (403 bp) were used to assess phylogenetic relationships among 20 species of Ctenomys and 3 octodontid species. Some of the main groups of Ctenomys species previously reported in the literature (e.g., the “boliviensis” group) are confirmed, as is the lack of resolution of basal nodes. This star-like pattern of diversification of tuco-tucos was recovered with both the new nuclear dataset and an expanded mitochondrial dataset, providing further evidence that Ctenomys underwent a phase of rapid diversification early in its history.

Species groups and the evolutionary diversification of tuco-tucos, genus Ctenomys (Rodentia: Ctenomyidae)

Abstract We present the most comprehensive study to date of species groups in Ctenomys (tuco-tucos), a species-rich genus of Neotropical rodents. To explore phylogenetic relationships among 38 species and 12 undescribed forms we sequenced the complete mitochondrial cytochrome-b genes of 34 specimens and incorporated 50 previously published sequences. Parsimony, likelihood, and Bayesian phylogenetic analyses were performed using additional hystricognath rodents as outgroup taxa. The basal dichotomy of Ctenomys splits C. sociabilis from the remaining tuco-tucos, within which 8 main species groups were identified: boliviensis, frater, mendocinus, opimus, magellanicus, talarum, torquatus, and tucumanus. Whereas most of these groups refer to previous clades proposed on the basis of chromosomes or morphology, the torquatus and magellanicus species groups are novel taxonomic hypotheses. However, relationships among species groups are poorly resolved. Furthmore, the positions of C. leucodon, C. maulinus, and C. tuconax are conflicting or unresolved, and they might represent additional independent lineages. On the basis of molecular dating, we estimate that most species groups originated approximately 3 million years ago.

ARE RATES OF DIVERSIFICATION IN SUBTERRANEAN SOUTH AMERICAN TUCO-TUCOS (GENUS CTENOMYS, RODENTIA : OCTODONTIDAE) UNUSUALLY HIGH?

Subterranean rodents have been used frequently as examples of explosive speciation in mammals. We tested for differential rates of diversification by using information from molecular phylogenies to focus primarily on tuco‐tucos (Rodentia: Octodontidae), the most speciose lineage of subterranean rodents. Tuco‐tucos were not significantly more diverse than their sister taxon (octodontines); however, a lineages‐through‐time analysis suggests an increase in diversification at the base of the tuco‐tuco clade.

Cytogenetics and Morphology of Ctenomys torquatus (Rodentia: Octodontidae)

Two chromosomal forms of Ctenomys torquatus are found in southern Brasil: 2n = 44 and 2n = 46, both showing AN = 72. The patterns of the G and C bands and the nucleolar organizer regions are presented. The two chromosomal forms do not show important differences in their morphology.

Evolutionary History of the Arctic Ground Squirrel (Spermophilus parryii) in Nearctic Beringia

Abstract Pleistocene glaciations had significant effects on the distribution and evolution of arctic species. We focus on these effects in Nearctic Beringia, a high-latitude ice-free refugium in northwest Canada and Alaska, by examining variation in mitochondrial cytochrome b (Cytb) sequences to elucidate phylogeographic relationships and identify times of evolutionary divergence in arctic ground squirrels (Spermophilus parryii). This arctic-adapted species provides an excellent model to examine the biogeographic history of the Nearctic due to its extensive subspecific variation and long evolutionary history in the region. Four geographically distinct clades are identified within this species and provide a framework for exploring patterns of biotic diversification and evolution within the region. Phylogeographic analysis and divergence estimates are consistent with a glacial vicariance hypothesis. Estimates of genetic and population divergence suggest that differentiation within Nearctic S. parryii occurred as early as the Kansan glaciation. Timing of these divergence events clusters around the onset of the Kansan, Illinoian, and Wisconsin glaciations, supporting glacial vicariance, and suggests that S. parryii survived multiple glacial periods in Nearctic Beringia. Across the Arctic, Beringia has been identified as an important regional refugium for a number of species. Within Nearctic Beringia, genetic differentiation across populations of arctic ground squirrels further reflects the effect of glacial patterns on a finer scale. The arctic ground squirrel has had a long evolutionary history in the Nearctic, with strong phylogeographic structure and stable clades persisting through multiple glacial cycles.

Phylogeographical structure in the subterranean tuco‐tuco Ctenomys talarum (Rodentia: Ctenomyidae): contrasting the demographic consequences of regional and habitat‐specific histories

In this work we examined the phylogeography of the South American subterranean herbivorous rodent Ctenomys talarum (Talas tuco‐tuco) using mitochondrial DNA (mtDNA) control region (D‐loop) sequences, and we assessed the geographical genetic structure of this species in comparison with that of subterranean Ctenomys australis, which we have shown previously to be parapatric to C. talarum and to also live in a coastal sand dune habitat. A significant apportionment of the genetic variance among regional groups indicated that putative geographical barriers, such as rivers, substantially affected the pattern of genetic structure in C. talarum. Furthermore, genetic differentiation is consistent with a simple model of isolation by distance, possibly evidencing equilibrium between gene flow and local genetic drift. In contrast, C. australis showed limited hierarchical partitioning of genetic variation and departed from an isolation‐by‐distance pattern. Mismatch distributions and tests of neutrality suggest contrasting histories of these two species: C. talarum appears to be characterized by demographic stability and no significant departures from neutrality, whereas C. australis has undergone a recent demographic expansion and/or departures from strict neutrality in its mtDNA.