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Caviomorph rodents: an introduction A.I. Vassallo and C.D. Antenuchi Aims and scope. This book covers aspects of evolutionary history and adaptive diversity of a group of rodents known as caviomorph, one of whose main features is that they evolved in South America, where it probably arrived from Africa. But in addition to focusing on a particular group of animals, this book aims to address general issues related to evolutionary biology. We asked the following question: what light may be shed the study of caviomorph on certain ecological evolutionary processes? Evolutionary biology is perhaps one of the most integrative disciplines of biology, as it draws on disciplines such as morphology, ecology, genetics, physiology, behavior, and biogeography. So, the study of a particular taxonomic group but integrating different disciplines could help to answer more general questions concerning evolution. By themselves, rodents are extremely diverse, including more than 2000 living species; therefore it is the order of mammals with the largest number of species. In addition to the quantitative side, because their contribution to the large number of species included into to the Order Rodentia, caviomorph have a huge adaptive diversity. This diversity is probably the outcome of the ability of this group to respond to environmental challenges with very different morphological, physiological and behavioral adaptations, which have given rise to a great diversity of ecological niches. The extent of these adaptations seems to overcome qualitatively those that are seen not only in the remaining groups of rodents, but also in various groups of mammals. This leads to the fact that the image, or physiognomy of what is usually considered a typical rodent (e.g. Rattus; Mus; squirrel) differs greatly from the picture we get when we look a mara, a capybara, or a tuco tuco. When we study the diversity and evolution of a particular group of organisms, there are today very different disciplines with their methodologies, allowing increasingly narrow questions to answer. However, it has been said that species evolve as a whole, responding in some way with all their "phenotypic and genotypic baggage?. One can hardly wonder about the adaptive value of a particular trait isolated and detached from the rest of the features of the species. In this book we have gathered a number of studies on the biology of caviomorph rodents because we have the opinion that their study has advanced significantly thanks to the different biological disciplines. We believe it is time to attempt a new synthesis or integration of the different contributions. We want to mention here the excellent book ?The biology of hystricognath rodents? (1974), by BarbaraWeir and Rowlands, which is one of the most important background on this group of rodents. The Order Rodentia A brief account of the knowledge about the origin of this order is necessary to bring us subsequently in the study caviomorphs. Most of the nearly 28 families of rodents appeared as part of a rapid cladogenesis during the late Eocene. North American extinct forms from the late Paleocene, known as ischyomyids, are considered basal rodents. These forms have the typical dentition comprising two incisors in each jaw, with a double layer of enamel on the labial side. The genus Paramys would be one of these extinct basal forms (Kemp xxx). This family diversified during the Eocene in North America, Eurasia and Africa being probably the stem group of the infraorders Sciuromorpha (squirrels) and Myomorpha (mice). According to Kemp (and references therein, see also Antoine et al. 2011), the primitive genus Cocomys from China has affinities in their dentition with the third major rodent infraorder, Hystricomorpha. A recent analysis based on extant species using molecular characters (Fabre et al 2012; Fig. 3 in Antoine et al., Fig. 1) shows results largely consistent with those based on dental characters from extinct forms (e.g. Marivaux et al. 2004). These studies show the existence of three major clades within Rodentia: a clade related to squirrels, the mice related clade, and the clade called Ctenohystrica (Hystricomorpha + Phimorpha [African mole rats, Old World porcupines] + Ctenodactiloidea). Hystricomorpha, histricognathi and Caviomorpha: some terminological issues. So-called Hystricomorpha rodents have a particular arrangement of the masseteric musculature consistent in the presence of a branch of the masseter muscle, called medial masseter, which passes through the infraorbital foramen (Fig. 2). This branch of the masseter muscle arises from the sides of the diastema (the anterior face of rodents). On the other hand, so-called Hystricognathi rodents have the particular condition in the lower jaw in which the angle of the jaw is lateralized regarding incisors (Fig. 3). This group includes living and extinct, both African and South American forms. The latter are known as Caviomorpha (= South American Hystricognathi). How caviomorph originate? The most accepted hypothesis is that they dispersed from Africa to South America, through some kind of strategy that could include the crossing of the sea on floating debris or vegetation. Note that the distance between the two continents by the time that occurred this dispersion, 35-41 million years ago, was substantially shorter than the observed today but anyway they had to cross a large body of water (Fig. 4 from http://cpgeosystems.com/paleomaps.html Dr. Ronald Blakey). The study by Antoine et al. (2011) reported the fossil remains of several species of basal caviomorph, dated 41 million years ago, and belonging to the Formation Yahuarango in Perú. This study represents a shift backward in the date of appearance of the first forms of caviomorph rodents, suggesting that the arrival and early evolution of the group may have occurred at a time characterized by relatively warm and humid climates around the Mid-Eocene Climatic Optimum, compared with the cooling that characterized the Eocene / Oligocene (approx. 34 Mya). Apparently these were animals that had small body size (40-120 g) compared to the further body mass diversification experienced by several lineages within the group. According to the authors, the moderate disparity in dental morphological characteristics evidenced by these extinct species suggests that they represent the early stages of group diversification in South America, which subsequently experienced a marked divergence of trophic apparatus regarding to very different types of diet and habits. Just like other groups of typical South American mammals (e.g. xenarthrans; notoungulates), it is often said that caviomorph rodents are endemic to this continent. Since its arrival from Africa ~40 million years ago, until the formation of the Isthmus of Panama only about 3 million years ago, the caviomorphs experienced, in isolation from other rodent groups, the vast diversification made manifest both by extant as well as extinct forms. During this extended period South America experienced major changes in its climate, which resulted in the modification of the environmental characteristics of many macro-regions. One of the biggest changes was the aridity and late Miocene global cooling, which particularly affected the south of South America, where open environments evolved. Caviomorphs accompanied these environmental changes, generating themselves --through different behavioral strategies and physiological adaptations-- new ecological niches. The two macrohabitats possessing higher density of species are represented today by the Amazon and the Atlantic Forest (CHAPTER Ojeda et al.). Evolutionary comrades. Obviously, no caviomorph group experienced its diversification in isolation from other mammal taxa that either were already present in South America, or arrived later (Fig. 5). They coexisted with other herbivorous mammals, for example the so-called extinct southamerican ungulates (Meridiungulata), which included larger animals like Macrauchenia (Orden Litopterna) and Toxodon (Orden Notoungulata), as well as rodentiform, small sized genera such as Paedotherium and Pachyrukhos (Orden Notoungulata). Even though eutherian carnivores (e.g. felids, canids, ursids) recently arrived at South America with the formation of the Isthmus of Panama ~3 million years ago, throughout much of their evolutionary history caviomorph coexisted with several big sized marsupial predators such as Borrhyena and Thylacosmilus. Caviomorph rodents coexist with xenarthrans whose main divergence between sloths, anteaters and armadillos has already occurred (according to recent dating based on molecular clock, Delsuc and Douzery, 2008) before the ancestors of caviomorph arrived at South America. Finally it should be mentioned the New World monkeys or Platyrrhini, who arrived at South America not long after the caviomorph. The diversification into five families experienced by this group took place almost in parallel with the diversification of caviomorph rodents (Pérez et al. 2013; Fig. 5). Role in South American ecosystems. Caviomorphs certainly play an important role in the ecological communities of South America. For example, studies have demonstrated the importance of agouti Dasyprocta leporina in seed dispersal in the Atlantic forest ecosystems, environments where this seems to fill the role played in the past by frugivorous extint mammals during the late Pleistoceno (Galetti et al., 2010). In this volume the role of caviomorfos is analyzed as prey species of carnivorous mammals and raptors (CHAPTER Zapata et al.). Among other findings, this chapter shows that the frequency of occurrence of species of larger body size, as Hydrochoerus sp and Dasyprocta spp, in the diet of certain carnivores sometimes exceeds the value of 60%, which clearly indicates its importance as prey. Strikingly, this strong representation in the diet of carnivores and raptors is also observed in forms such as the subterranean genus Ctenomys whose peculiar lifestyle would not appear to substantially protect them from predation but as a way to save energy for thermorregulation. It is also surprisingly, that social life style does not prevent predation when compared with solitary species, and diurnal social species were more predated than nocturnal. Locomotion, size, and shape. The body plan of rodents allows this group an important generalism in terms of the environments that they can inhabit. In general, rodents are able to travel with a moderate skill in different habitats. Take, for example, what might be considered a typical representative of the Order Rodentia, Rattus. It is known that rats can swim well, they are able to climb and dig caves, also moving fast on land. There are species of rodents that are more specialized to particular types of locomotion and habitats. For instance, squirrels (Sciurus) are very good climbers, beavers (Castor) are very good swimmers, while pocket gophers (Geomys) are excellent diggers. However, caviomorphs seem to have reached even great ecological diversification which is reflected largely on the structure of the post cranial skeleton (CHAPTER Morgan et al.). No other group of rodents reached the diversity of body sizes seen in the caviomorphs. If we look at the extant forms that is evident when comparing the body size of a coruro (Sapalacopus cyanus), whose mass is around 150 g, respect to a carpincho (capybara), which can weigh up to 60 kg. This diversity becomes even more evident when extinct forms whose estimated weight is ~700 kg are taken into account (e.g. Josephoartigasa monesi). Why this group has reached such a disparity in body size? External causes have been invoked as the existence of vacant niches because South America had no native modern ungulates (they arrived to South America about 3 million years after the formation of the Isthmus of Panama). However it cannot be ruled out internal causes, such as the existence of marked size evolvability due to factors regulating size growth during ontogeny (e.g. Berstein et al 2007). Many caviomorphs are able to climb, an example would be the spiny rats (spiny tree-rats, tree-rats, bamboo-rats) and porcupine (Erethizon) from Central and South America. When comparing other species, it is clear that evolution led to a dichotomy in limb morphology. In some species the limb are elongated and hence adapted for speed, while in others they adapted for strength, in which case they are short and stout. With regard to the ability to fast locomotion, both maras (Dolichotis) and pacas (Dasyprocta) have reached an important degree of specialization that allows them to run fast in the open environments of Patagonia as well as environments with dense vegetation, showing several convergences with the small ungulates (Rocha Barbosa et al. CHAPTER). Strong and robust limbs, on the other hand, are characteristic of swimmers like the semiaquatic coipo (Myocastor) and diggers as degus (Octodon), tuco-tucos (Ctenomys), and (Spalacopus) coruros. Behavior. The group shows a significant diversity in aspects of behavior, particularly in relation to the degree of sociality (CHAPTER Herrera). There are several different mating systems among caviomorph rodents, which include monogamy and communal care of offspring in the case of maras, and solitary behavior and polygyny in the subterranean rodent Ctenomys; and polygyny in conjunction with a certain degree of herding in Cavia pamparum. Capybaras form stable groups of 10 to 20 individuals of both sexes, which defend a common territory. On the other hand, vizcachas live in colonies consisting of 1-2 adult males and 1-2 adult females and their young. Females are philopatric, meaning that at the time of natal dispersal remain in the vicinity of the colony, while males disperse to greater distances. Genetic studies. The use of molecular techniques has helped to address quite different questions regarding the biology of caviomorphs. On the one hand, gene sequencing has provided an enormous amount of characters which, in conjunction with those provided by the morphological study of current and extinct forms have enabled the production of robust phylogenies of the different caviomorph lineages. The sequencing of other genes has allowed, on the other hand, answer questions about the relationship between intraspecific diversity at the population level, and its relationship to geography, within the framework of a relatively new discipline known as phylogeography. The use of another type of genetic material (e.g. microsatellites) has been helpful to explore both reproductive behavior (through allowing knowing the paternity of offspring in natural populations) and the dispersal of individuals, two key demographic issues (Mora et al. 2010, Zenuto et al.1999). In addition to studies on the evolution of insulin and major histoincompatibility complex genes, caviomorph provide an interesting model for the implementation of massive sequencing techniques which allow addressing new questions, as showed by (CHAPTER MacManes et al.). In this regard caviomorphs have had the greatest role for physiological researches as study models. It would be impossible to describe in this introduction the role of this group but, only to take a into a count the quantitative and qualitative importance of its contribution, if we search for Guinea pig ?a caviomorph´s species only- on a diffused scientific database, at the time we are writing these lines, the search shed 12,093 papers.As an example, among its physiological distinctiveness, this group of rodents has a divergent insulin structure, as was pointed out by Opazo and coworkers (2005). Insulin in this group of rodents exhibits only 1?10% of biological activity in comparison to other mammals. Therefore, hystricomorph rodents may hypothetically be unable to regulate blood glucose concentration as nonhystricomorph mammals. Because its diverse habitat use which includes distinctive adaptation traits, as was noted above, caviomorph occupy so different ambient that shows remarkably diverse physiological adaptations. A conspicuous example is represented by subterranean forms belonging to Ctenomys genus, that has been extensively studied. Other than the morphological adaptation to dig, it shows blood adaptation to hypoxia and hypercapnia, low basal metabolic rates that have been relate to avoiding overheating, distinctive chemical and sound communication, etc. Recently, caviomorph genus as Octodon and Ctenomys have been used as models for the study of stress axis both, in captivity and in the wild. Studies evaluating the effect of stressors on learning capabilities and immunological system are being held in Ctenomys, which represent a promising field of research to the understanding the biological meaning of stress responses.In this volume, a chapter on energetic, aims to searching for energetic patterns within caviomorphs rodents and other explores reproductive patterns within this group. We hope that this volume can provide a comprehensive overview of the main research lines on caviomorph rodents, and that it promotes interest and enthusiasm in continuing their study. Acknowledgments. We greatly appreciate the support received by the SAREM (Sociedad Argentina para el Estudio de los Mamíferos) since the start of this project, and all our colleagues with whom we share discussions, conferences, and unforgettable dinners (many of them during the fieldwork). Grant sponsors PIP 1380 (CONICET); PICT 2121 (ANPCyT) (AIV). 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DNA fingerprinting reveals polygyny in the subterranean rodent Ctenomys talarum. Molecular Ecology 8: 1529?1532. FIGURE LEGENDS Fig. 1 Time scale for rodent diversification. Modified from Fabre et al. (2012). Fig. 1 Escala de tiempo de la diversificación de los roedores. Modificado de Fabre et al. (2012). Fig. 2 The hystricomorph condition as seen in Ctenomys. Fig. 2 La condición (estado) hystricomorpha, ejemplificada con Ctenomys. Fig. 3 Sciurognath (A) and hystricognath (B) condition. In the former condition the angular process of the jaw (dark grey) almost coincides with a plane passing through the alveolus of the incisors (dotted line). In the second condition the angular process is lateral with respect to that plane. Modified from Hautier et al. 2011. Fig. 3 La condición sciurognatha (1) e hystricognatha (2). En la primera condición el proceso angular de la mandíbula (gris oscuro) coincide mayormente con el plano que pasa por el alvéolo de los incisivos (línea punteada). En la segunda, el proceso angular es lateral respecto a dicho plano. Modificado de Hautier et al. 2011. Fig. 4. Continental masses at hystricomorph arrival to South America (above) and at presente (below). From http://cpgeosystems.com/paleomaps.html Dr. Ronald Blakey. Fig. 4. Posición de las continentes en la época del arribo de los hystricomorfos a Sud América (arriba) y actualmente (abajo). Tomado de http://cpgeosystems.com/paleomaps.html Dr. Ronald Blakey. Fig. 5. Time scale of the diversification of various lineages of mammals in southamerica. Based on different sources (Delsuc and Douzery 2008; Upham and Patterson (this book); Meredith et al. 2008; Pérez et al. 2013). Fig. 5 Escala de tiempo de la diversificación de varios linajes de mamíferos sudamericanos. Basado en varias fuentes (Delsuc and Douzery 2008; Upham and Patterson (this book); Meredith et al. 2008; Pérez et al. 2013).