Helder Gomes Rodrigues

Dental microwear patterns of extant and extinct Muridae (Rodentia, Mammalia) : ecological implications

Extant species of Muridae occupy a wide array of habitats and have diverse dietary habits. Consequently, their dental microwear patterns represent a potential clue to better understand the paleoecology of their extinct relatives, which are abundant in many Old World Neogene localities. In this study, dental microwear is investigated for specimens of 17 extant species of murine and deomyine rodents in order to test the reliability of this method and infer dietary preferences on the fossil species Saïdomys afarensis. This extinct form comes from a mid-Pliocene site (AL 327) located at the Hadar Formation (Ethiopia) known to have delivered many hominid specimens of Australopithecus afarensis. A significant correlation between microwear patterns and diet is detected. Thus, grass, fruit, and insect eaters display, respectively, high amounts of fine scratches, wide scratches, and large pits. Moreover, some aspects of the paleoecology of S. afarensis, including feeding habits, could be assessed in regard to its dental microwear pattern. Indeed, it probably had feeding habits similar to that of living grass eaters. These results concur with the presence of open to woodland areas covered by an herbaceous vegetal layer, including monocotyledons, in the vicinity of this mid-Pliocene locality.

Anthropoid versus strepsirhine status of the African Eocene primates Algeripithecus and Azibius: craniodental evidence.

Recent fossil discoveries have demonstrated that Africa and Asia were epicentres for the origin and/or early diversification of the major living primate lineages, including both anthropoids (monkeys, apes and humans) and crown strepsirhine primates (lemurs, lorises and galagos). Competing hypotheses favouring either an African or Asian origin for anthropoids rank among the most hotly contested issues in paleoprimatology. The Afrocentric model for anthropoid origins rests heavily on the >45 Myr old fossil Algeripithecus minutus from Algeria, which is widely acknowledged to be one of the oldest known anthropoids. However, the phylogenetic position of Algeripithecus with respect to other primates has been tenuous because of the highly fragmentary fossils that have documented this primate until now. Recently recovered and more nearly complete fossils of Algeripithecus and contemporaneous relatives reveal that they are not anthropoids. New data support the idea that Algeripithecus and its sister genus Azibius are the earliest offshoots of an Afro–Arabian strepsirhine clade that embraces extant toothcombed primates and their fossil relatives. Azibius exhibits anatomical evidence for nocturnality. Algeripithecus has a long, thin and forwardly inclined lower canine alveolus, a feature that is entirely compatible with the long and procumbent lower canine included in the toothcomb of crown strepsirhines. These results strengthen an ancient African origin for crown strepsirhines and, in turn, strongly challenge the role of Africa as the ancestral homeland for anthropoids.

Continuous dental replacement in a hyper-chisel tooth digging rodent

Contrary to their reptilian ancestors, which had numerous dental generations, mammals are known to usually develop only two generations of teeth. However, a few mammal species have acquired the ability to continuously replace their dentition by the constant addition of supernumerary teeth moving secondarily toward the front of the jaw. The resulting treadmill-like replacement is thus horizontal, and differs completely from the vertical dental succession of other mammals and their extinct relatives. Despite the developmental implications and prospects regarding the origin of supernumerary teeth, this striking innovation remains poorly documented. Here we report another case of continuous dental replacement in an African rodent, Heliophobius argenteocinereus, which combines this dental system with the progressive eruption of high-crowned teeth. The escalator-like mechanism of Heliophobius constitutes an original adaptation to hyper-chisel tooth digging involving high dental wear. Comparisons between Heliophobius and the few mammals that convergently acquired continuous dental replacement reveal that shared inherited traits, including dental mesial drift, delayed eruption, and supernumerary molars, comprise essential prerequisites to setting up this dental mechanism. Interestingly, these dental traits are present to a lesser extent in humans but are absent in mouse, the usual biological model. Consequently, Heliophobius represents a suitable model to investigate the molecular processes leading to the development of supernumerary teeth in mammals, and the accurate description of these processes could be a significant advance for further applications in humans, such as the regeneration of dental tissues.

Roles of dental development and adaptation in rodent evolution

In paleontology, many changes affecting morphology, such as tooth shape in mammals, are interpreted as ecological adaptations that reflect important selective events. Despite continuing studies, the identification of the genetic bases and key ecological drivers of specific mammalian dental morphologies remains elusive. Here we focus on the genetic and functional bases of stephanodonty, a pattern characterized by longitudinal crests on molars that arose in parallel during the diversification of murine rodents. We find that overexpression of Eda or Edar is sufficient to produce the longitudinal crests defining stephanodonty in transgenic laboratory mice. Whereas our dental microwear analyses show that stephanodonty likely represents an adaptation to highly fibrous diet, the initial and parallel appearance of stephanodonty may have been facilitated by developmental processes, without being necessarily under positive selection. This study demonstrates how combining development and function can help to evaluate adaptive scenarios in the evolution of new morphologies.

Zegdoumyidae (Rodentia, Mammalia), stem anomaluroid rodents from the Early to Middle Eocene of Algeria (Gour Lazib, Western Sahara): new dental evidence

The Palaeogene fossil record of rodents in Africa is very poor compared to that of North America or Eurasia. Despite this, Africa has long appeared to be a centre of adaptive radiation for two distinct groups of Rodentia: Hystricognathi and Anomaluroidea. The >45-million-year-old enigmatic Zegdoumyidae is the oldest and only rodent family known of this age from Africa (Algeria and Tunisia). Zegdoumyids have been tentatively regarded as a possible early African stem group for Anomaluridae, a link that has never been clearly established because of the highly fragmentary nature of zegdoumyid fossils, as well as the major temporal and morphological gaps between zegdoumyids and the first true anomaluroids from the Late Eocene. About 200 rodent teeth have been sorted after acid treatment of indurated sediments from several new localities in the Gour Lazib of western Algeria dating from the late Early or early Middle Eocene. These new fossils allow us to better describe the morphology of the Zegdoumyidae (especially Glibia and Zegdoumys) and to identify a new taxon, Lazibemys zegdouensis gen. et sp. nov. With this material, we investigated the phylogenetic position of the Zegdoumyidae in a high-level rodent phylogeny with cladistic assessment of the dental evidence. Our analyses have yielded six equally most-parsimonious trees in which zegdoumyids represent the earliest offshoots (pectinately arranged) of a large clade that embraces Eocene anomaluroids plus stem and crown Anomaluridae. This phylogenetic assumption underscores the great antiquity of the Anomaluroidea clade in Africa, as expected given the high morphological divergence of the Late Eocene African anomaluroids. Zegdoumyids exhibit a variety of dental morphologies and provide some suggestions on evolutionary trends within the Anomaluroidea (early stages of pentalophodonty, incisor enamel microstructure transitional from the pauciserial to the uniserial condition). The source of Zegdoumyidae is still unclear inasmuch as there is no well-identified sister group among early Palaeogene rodents. Zegdoumyids seem to share a common ancestry with both stem Myodonta and North American Sciuravidae. Given the high degree of dental specialization of zegdoumyids, we cannot exclude the possibility that zegdoumyids are rooted in a more primitive, as yet unknown, African rodent lineage older than the Early-Middle Eocene.

UNDER PRESSURE? DENTAL ADAPTATIONS TO TERMITOPHAGY AND VERMIVORY AMONG MAMMALS

The extant mammals have evolved highly diversified diets associated with many specialized morphologies. Two rare diets, termitophagy and vermivory, are characterized by unusual morphological and dental adaptations that have evolved independently in several clades. Termitophagy is known to be associated with increases in tooth number, crown simplification, enamel loss, and the appearance of intermolar diastemata. We observed similar modifications at the species level in vermivorous clades, although interestingly the vermivorous mammals lack secondarily derived tools that compensate for the dentitions reduced function. We argue that the parallel dental changes in these specialists are the result of relaxed selection on occlusal functions of the dentition, which allow a parallel cascade of changes to occur independently in each clade. Comparison of the phenotypes of Rhynchomys, a vermivorous rat, and strains of mice whose ectodysplasin (EDA) pathway has been mutated revealed several shared dental features. Our results point to the likely involvement of this genetic pathway in the rapid, parallel morphological specializations in termitophagous and vermivorous species. We show that diets or feeding mechanisms in other mammals that are linked to decreased reliance on complex can lead to similar cascades of change.

Diet of the extinct Lava mouse Malpaisomys insularis from the Canary Islands: insights from dental microwear

Malpaisomys insularis is a mouse-like rodent endemic to the eastern Canary Islands. It became extinct during the fourteenth century. It was a remarkable species living under hyperarid conditions. A dental microwear analysis was performed in order to determine its former diet. The elevated number of fine scratches found in Malpaisomys molars suggests that it consumed a significant part of Poaceae, grass consumption leaving the most distinctive features on dental wear facets. A graminivorous diet with a high amount of abrasive items is in agreement with the broad teeth of Malpaisomys, considered as adapted to grass consumption. However, in the absence of potential competitors over its native range, it is likely that Malpaisomys also foraged on dicots to meet higher nutrient and energetic requirements. The ecology of Malpaisomys is discussed from these results in the context of the desertic climatic conditions of the eastern Canary Islands and with a special concern on its small body size in contrast to other large-sized island murine species such as the giant rats of the central Canary Islands.

Early adaptive radiations of Aplodontoidea (Rodentia, Mammalia) on the Holarctic region: systematics, and phylogenetic and paleobiogeographic implications

The Aplodontoidea, now restricted to only one North American species (Aplodontia rufa), have shown a wide Holarctic extension since the Upper Eocene. As their fossil record is poor, their phylogenetic relationships and the origins of their successive radiations remain unclear. We perform here phylogenetic analyses, primarily based on dental evidence (94 dental of 97 characters), restricted to Paleogene and early Miocene taxa (46 taxa) in order to avoid biases introduced by substantially derived (divergent) taxa. We confirm the inclusion of some problematic genera such as Cedromus or Douglassciurus within Sciuroidea rather than in Aplodontoidea. Ephemeromys and Lophallomys appear as the most basal members of the Aplodontoidea, and Epeiromys is the closest outgroup of the Sciuroidea-Aplodontoidea clade. The relationships among the “prosciurines” remain unclear, with paraphyletic genera such as Prosciurus and Haplomys. Their diagnoses are reevaluated and a new genus is described. The Aplodontidae, including the clade of the latter, and Haplomys liolophus display a dichotomy between Ansomyinae and Aplodontinae, the two crown groups. The first clade formed by the European species argoviensis and descendens (referred to a new genus) can be proposed as a sister group of the species of Ansomys. The second branch of the dichotomy includes the European Plesispermophilus and Sciurodon as basal groups. The species of Parallomys do not form a clade, and the genus appears paraphyletic. The last dichotomy separates the Allomys clade from the ‘meniscomyine’ clade. Comparisons of the selected species allow consideration of their patterns of dental evolution (e.g. enlargement of P4, development of a metaloph—protoloph disto-mesial connection, of crescentic shape in main cusps and ectoloph, of a buccal protruding compressed mesostyle, of a metastylid crest or an anterior spur of the hypoconid, etc.). The split between sciuroids and aplodontoids occurred in North America, and then aplodontoids dispersed rapidly throughout the whole Holarctic region. The first aplodontid adaptive radiation took place either in North America or in Asia. Periodic exchanges occurred between Europe, Asia and North America, and the last radiations (meniscomyines) were restricted in North America.KurzfassungDie Aplodontoidea waren seit dem Ober-Eozän holarktisch weit verbreitet, sind heute aber auf eine nordamerikanische Art (Aplodontia rufa) beschränkt. Da ihre fossilen Belege spärlich sind, bleiben ihre phylogenetischen Beziehungen sowie die Wurzeln ihrer aufeinander folgenden Radiationen unklar. Wir haben eine phylogenetische Analyse der Aplodontoidea durchgeführt, die in erster Linie auf Zahnmerkmalen basiert (94 von 97 Merkmalen). Die Auswahl der Taxa ist auf das Paläogen und frühe Miozän beschränkt (46 Taxa), um eine Verzerrung durch stark abgeleitete (divergente) Taxa zu vermeiden. Nach unserer Analyse gehören einige bisher fragliche Sciuroidea wie Cedromus oder Douglassciurus tatsächlich in diese Gruppe und nicht zu den Aplodontoidea. Ephemeromys und Lophallomys erweisen sich als ursprünglichste Mitglieder der Aplodontoidea, und Epeiromys stellt die Schwestergruppe des von Sciuroidea und Aplodontoidea gebildeten Taxons dar. Die Beziehungen zwischen den “Prosciurinen” bleiben unklar mit paraphyletischen Gattungen wie Prosciurus und Haplomys. Ihre Diagnosen werden revidiert und eine neue Gattung wird beschrieben. Die Aplodontidae inklusive der neuen Gattung und von Haplomys liolophus bilden eine Dichotomie mit Ansomyinae und Aplodontinae. Der erste Zweig, der aus den europäischen Arten argoviensis und descendens (zu einer neuen Gattung gestellt) besteht, bildet die Schwestergruppe zur Gattung Ansomys. Der zweite Ast der Dichotomie umfasst den europäischen Plesispermophilus und auch Sciurodon als basale Gruppen. Die Arten von Parallomys stellen kein Monophylum dar, und die Gattung erscheint paraphyletisch. Die letzte Dichotomie trennt den Allomys-Zweig von dem ‘meniscomyinen’ Zweig. Ein Vergleich der ausgewählten Arten zeigt die evolutiven Veränderungen im Gebiss (z.B. Vergrößerung des P4, Entwicklung einer disto-mesialen Verbindung zwischen Metaloph und Protoloph, eines bogenförmigen Verlaufs von Haupthöckern und Ectoloph, eines Metastylid-Grates oder eines anterioren Vorsprungs des Hypoconids usw….). Die Aufspaltung von Sciuroiden und Aplodontoiden erfolgte in Nordamerika, und darauf verbreiteten sich die Aplodontoiden im gesamten holarktischen Bereich. Die erste adaptive Radiation der Aplodontoiden erfolgte entweder in Nordamerika oder in Asien. Es kam zu wiederholtem Austausch zwischen Europa, Asien und Nordamerika, aber die letzten Radiationen (Meniscomyinen) waren auf Nordamerika beschränkt.

Life in Burrows Channelled the Morphological Evolution of the Skull in Rodents: the Case of African Mole-Rats (Bathyergidae, Rodentia)

African mole-rats are fossorial rodents that consist of five chisel-tooth digging genera (Heterocephalus, Heliophobius, Georychus, Fukomys, and Cryptomys) and one scratch digger (Bathyergus). They are characterized by striking physiological, morphological, and behavioral adaptations intimately related to their subterranean life. The influence of their mode of life in shaping the cranial morphology has yet to be evaluated in comparison to other Ctenohystrica, especially fossorial genera, which include the subterranean genera Spalacopus and Ctenomys. In our study, we seek to determine to what extent subterranean life affects the morpho-functional properties of the skull among fossorial ctenohystricans. 3D geometric morphometric analyses were performed on 277 skulls, encompassing 63 genera of Ctenohystrica, and complemented by biomechanical studies. African mole-rats and other subterranean Ctenohystrica, especially chisel-tooth diggers, have a short snout, a wide cranium with enlarged zygomatic arches, and a strongly hystricognathous mandible. Even if convergences are also manifest between most fossorial Ctenohystrica, subterranean rodents departed from the main ctenohystrican allometric trends in having a skull shape less size-dependent, but under stronger directional selection with intense digging activity as a major constraint. African mole-rats, notably chisel-tooth diggers, show important mechanical advantage for the temporalis muscles favoring higher forces at the bite point, while mechanical advantage of the superficial masseter muscles is lower compared to other Ctenohystrica. If subterranean species can be clearly discriminated based on their skull morphology, the intrinsic mosaic of anatomical characters of each genus (e.g., skull, teeth, and muscles) can be understood only in the light of their ecology and evolutionary history.

Ontogenetic and life history trait changes associated with convergent ecological specializations in extinct ungulate mammals

Significance Estimating life history traits such as pace of growth or longevity is difficult in extinct mammals. Yet, these parameters could be helpful to better understand how herbivorous mammals adapted to changing environments. We here highlight the insights gained by studying dental growth and eruption in a clade of extinct ungulate mammals. Variation in these traits was assessed in the context of volcanism, cooling, and increasing aridity in South America starting 50 Ma. We show that ever-growing teeth combined with faster molar eruption arose several times during the evolution of these mammals, allowing them to obtain a more durable and efficient dentition in constraining environments. These innovations might represent convergent ontogenetic and physiological adjustments that contributed to their ecological specialization. Investigating life history traits in mammals is crucial to understand their survival in changing environments. However, these parameters are hard to estimate in a macroevolutionary context. Here we show that the use of dental ontogenetic parameters can provide clues to better understand the adaptive nature of phenotypic traits in extinct species such as South American notoungulates. This recently extinct order of mammals evolved in a context of important geological, climatic, and environmental variations. Interestingly, notoungulates were mostly herbivorous and acquired high-crowned teeth very early in their evolutionary history. We focused on the variations in crown height, dental eruption pattern, and associated body mass of 69 notoungulate taxa, placed in their phylogenetic and geological contexts. We showed that notoungulates evolved higher crowns several times between 45 and 20 Ma, independently of the variation in body mass. Interestingly, the independent acquisitions of ever-growing teeth were systematically accompanied by eruption of molars faster than permanent premolars. These repeated associations of dental innovations have never been documented for other mammals and raise questions on their significance and causal relationships. We suggest that these correlated changes could originate from ontogenetic adjustments favored by structural constraints, and may indicate accelerated life histories. Complementarily, these more durable and efficient dentitions could be selected to cope with important ingestions of abrasive particles in the context of intensified volcanism and increasing aridity. This study demonstrates that assessing both life history and ecological traits allows a better knowledge of the specializations of extinct mammals that evolved under strong environmental constraints.