Ecological Physiology and Behavior in the Genus Ctenomys

FANJUL MARÍA SOL; CUTRERA ANA PAULA; LUNA FACUNDO; SCHLEICH, CRISTIAN E.; BRACHETTA VALENTINA; ANTENUCCI DANIEL; ZENUTO, ROXANA R.

Tuco-Tucos, An Evolutionary Approach to the Diversity of a Neotropical Subterranean Rodent

Springer, Cham

Año: 2021; p. 1 - 279

Such begin Darwin?s comments on tuco-tucos, based on his encounters withthese animals along the southern coast of Uruguay. Now, 175 years after the originalpublication of Darwin?s observations, biologists continue to be fascinated by thesecharismatic rodents. In part, this interest reflects the somewhat mysterious nature oftuco-tucos?even in areas where the animals are locally abundant and can at timesbe heard calling from all directions, it is often challenging to catch a glimpse ofthese largely subterranean mammals. Increasingly, though, interest in tuco-tucosreflects our growing understanding of the biology of these animals and the unexpectedwealth of phenotypic and genotypic variation that they represent. Indeed, asevident from the contents of this volume, studies of tuco-tucos now encompassanalyses of systematic, phylogenetic, morphological, physiological, ecological, andbehavioral diversity, providing important opportunities to examine the evolutionaryprocesses underlying divergence within Ctenomys and, concomitantly, convergencebetween these and other lineages of subterranean rodents.One attribute of tuco-tucos that makes them both intriguing and at times challengingto study is the apparently rapid divergence of species within the genusCtenomys. As Diego Verzi and colleagues indicate (Chap. 1), while the familyCtenomyidae appears to date to the Oligocene, the single extant genus Ctenomyshas arisen much more recently, with current species-level diversification dating onlyto the early Pleistocene. This rapid burst of speciation has made it difficult to evaluatethe evolutionary relationships among species, as molecular genetic analyseshave often failed to reveal much phylogenetic structure, particularly for deepernodes within the genus. Indeed, as Guillermo D?Elía and co-authors state (Chap. 2),phylogenetic analyses of tuco-tucos are in many ways still in their infancy and willbenefit substantially from inclusion of additional data sets (e.g., genomic-levelsequencing) as well as more comprehensive sampling of putative species and species groups. At the same time, the rapid diversification within Ctenomys createsexciting opportunities to explore the evolutionary mechanisms underlying speciationin this lineage. The role of chromosomal rearrangements in promoting speciationhas been a particular focus for studies of tuco-tucos due to the often pronouncedkaryotypic differences among species, including those for which molecular geneticanalyses fail to detect marked differentiation. This theme is examined by Thales deFreitas (Chap. 3), who concludes that evidence for distinct processes of speciation(e.g., allopatric, sympatric, chromosomal) varies in relation to the time since divergenceamong different members of the genus Ctenomys.Geographically, tuco-tucos are widespread, occurring throughout much of sub-AmazonianSouth America. At the level of individual taxa, however, it has longbeen thought that allopatry dominates, with only a few examples of sympatry havingbeen identified within Ctenomys. To explore how local spatial relationshipsamong species translate into the genus-level distribution of these animals, RenanMaestri and Bruce Patterson (Chap. 4) characterize geographic variation in severalattributes of Ctenomys, including patterns of species richness and range size. Theseauthors report that although species ranges tend to be smaller in Ctenomys, theexclusivity of these ranges does not differ from that observed in other lineages ofcaviomorph rodents, providing no evidence that allopatry is particularly pronouncedamong tuco-tucos. Fernando Mapelli and colleagues (Chap. 5) add a genetic componentto analyses of geographic variation, arguing that landscape features mayimpact the demographic processes that shape patterns of genetic differentiationwithin and among species of Ctenomys. Their review suggests that landscape-levelgenetic variation reflects a baseline pattern of isolation by distance that is modifiedby a complex, species-specific interplay between geographic features, environmentalconditions, and demographic parameters.In terms of their gestalt, it has been suggested that if you have seen one tuco-tuco,you have seen them all. This quip reflects the general expectation that thechallenges associated with life in underground burrows have acted to constrain morphologicaland other forms of phenotypic diversification within Ctenomys. Asknowledge of these animals has increased, it has become increasingly apparent thatthey are more phenotypically diverse than has been appreciated. Morphologically,variation is evident for multiple cranial traits, and, as reported by Rodrigo Forneland co-authors (Chap. 6), this variation displays geographic but not phylogeneticsignal, suggesting that environmental conditions may play a critical role in shapingskull structure in these animals. One obvious environmental factor that may contributeto this variation is the difference in the soils in which the animals live. Asdescribed by Aldo Vassallo and colleagues (Chap. 7), although tuco-tucos rely primarilyon their forepaws to dig, they also routinely use their incisors to chew throughobstructions or loosen hard chunks of soil. Accordingly, the structure of both theforelimbs and the skull may vary with soil type, and, conversely, constraints on thebiomechanics of digging may preclude the animals from occupying particular soils.Soil may also be an important determinant of the underappreciated variation in pelagecoloration that occurs within Ctenomys. Using comparisons of overall pelagecolor as well as the structure of individual hairs, Gislene Goncalves (Chap. 8) argues that differences in coloration among species of tuco-tucos from the Atlantic coastsof Brazil and Argentina reflect selection imposed by differences in soil color, withcolor matching to local substrates serving to protect animals from predation whileactive on the surface.Interactions between individuals and their environments are also central to studiesof the ecology and physiology of Ctenomys. The role of tuco-tucos as ecosystemengineers is examined by Bruno Kubiak and Daniel Gailano (Chap. 9), who alsoconsider the effects of habitat parameters on species? distributions as well as spatialand social relationships among conspecifics. Although relevant data are lacking formany species, the emerging picture is one of greater than expected ecological andbehavioral variation within the genus. One critical aspect of a species? ecology is itsdiet, which can affect not only where animals occur on the landscape but also howthey acquire energy and nutrients, thereby providing a particularly direct linkbetween external conditions and intrinsic processes. Although all tuco-tucos areherbivorous, surprisingly few detailed studies of the animals? diets have been conducted.As Carla Lopes (Chap. 10) reports, the growing use of DNA sequencing offecal samples to characterize diets is creating new opportunities to examine dietaryvariation within and among members of the genus Ctenomys, including the role ofdiet partitioning in shaping the few examples of sympatry that have been reportedfor these animals. Maria Sol Fanjul and colleagues (Chap. 11) explore the innerworkings of tuco-tucos in greater detail, revealing how differences in habitat conditionsas well as differences in how individuals use their habitats contribute to adaptivelyimportant variation in multiple physiological systems, including processingof sensory information, response to external stressors, and regulation of both waterand energy balance. Extrinsically generated differences in physiology may be mediatedby variation in individual phenotypes (e.g., sex, reproductive status), therebyadding an additional layer of complexity to efforts in understanding how externalconditions shape the internal biology of tuco-tucos. In the final chapter of the volume,Cristina Matzenbacher and Juliana da Silva (Chap. 12) take a more appliedapproach to interactions between tuco-tucos and their environments by examiningthe role of these animals as bioindicators of environmental change, specifically theintroduction of heavy metals and other toxic compounds as a result of human activity.More generally, this discussion raises the issue of conservation of the genusCtenomys, thereby serving to connect the previous chapters to the increasinglyimportant need to ensure that members of this lineage are protected from an ever-growinglist of threats.In closing, one theme that resonates throughout this volume is diversity. Fromsystematic and phylogenetic revisions of Ctenomys to analyses of interactionsbetween the environment and specific physiological processes, it is clear that studiesof tuco-tucos are revealing new and sometimes unexpected patterns of diversificationin this relatively young clade of rodents. Coupled with an ever-growing suiteof analytical tools, this diversity creates novel opportunities to examine long-standingquestions regarding the biology of tuco-tucos. For example, efforts tounderstand the often marked karyotypic differences among otherwise closely relatedspecies should benefit from the use of genomic tools to identify the specific portions of the genome that are impacted by chromosomal rearrangements. Similarly, as ourability to characterize the genomic architecture of specific phenotypic traitsincreases, we will be better able to examine the genetic bases for adaptive traits suchas the specialized morphological features associated with digging. More generally,the expanding catalog of diversity within Ctenomys means that members of thisgenus are increasingly recognized as important models for research on a wide rangeof evolutionary topics, including studies that explore the effects of pathogen communitieson immunological function or the role of ecological factors in generatinginterspecific differences in social systems. All told, our growing understanding ofthe biology of tuco-tucos suggests that the ?curious small animals? that intriguedDarwin will continue to play a central role in biological research for years to come.