Diversity dynamics of Miocene mammals in relation to the history of tectonism and climate

Continental biodiversity gradients result not only from ecological processes, but also from evolutionary and geohistorical processes involving biotic turnover in landscape and climatic history over millions of years. Here, we investigate the evolutionary and historical contributions to the gradient of increasing species richness with topographic complexity. We analysed a dataset of 418 fossil rodent species from western North America spanning 25 to 5 Ma. We compared diversification histories between tectonically active (Intermontane West) and quiescent (Great Plains) regions. Although diversification histories differed between the two regions, species richness, origination rate and extinction rate per million years were not systematically different over the 20 Myr interval. In the tectonically active region, the greatest increase in originations coincided with a Middle Miocene episode of intensified tectonic activity and global warming. During subsequent global cooling, species richness declined in the montane region and increased on the Great Plains. These results suggest that interactions between tectonic activity and climate change stimulate diversification in mammals. The elevational diversity gradient characteristic of modern mammalian faunas was not a persistent feature over geologic time. Rather, the Miocene rodent record suggests that the elevational diversity gradient is a transient feature arising during particular episodes of Earth''s history.     

Seasonal Variations in the Expression of the mRNA Encoding ß1-Adrenoceptor and AA-NAT Enzyme,and in the AA-NAT Activity in the Pineal Gland of Vizcacha (Lagostomus maximus maximus) – Correlation With Serum Melatonin

The vizcacha is a photoperiodic rodent living in the southern hemisphere. The adult males exhibit an annual reproductive cycle characterized by a gonadal regression period during winter with, in some animals, an almost complete loss of spermatogenesis. In this study, we investigated whether biochemical parameters involved in melatonin synthesis in the vizcacha pineal gland exhibited an annual rhythm in parallel with the annual reproductive cycle. By use of in situ hybridization, an annual variation of mRNA encoding ß 1 -adrenoceptor was shown, with a maximum during autumn and winter. In situ hybridization for mRNA encoding AA-NAT enzyme also exhibited an annual rhythm with the lowest and highest levels in May and August, respectively. Likewise, in August the activity of arylalkylamine N-acetyltransferase enzyme also reached a maximum. Finally, dertermination of the serum concentrations of melatonin by use of radioimmunoassay showed an increase during winter. Moreover, our results are in concordance with several biochemical and morphological parameters of the reproductive axis of the male vizcacha, which support the reproductive rhythmicity of this rodent. Thus, our data suggest that the pineal gland and melatonin, which is activated via the sympathetic system, could be involved in the photoperiodically dependent annual reproductive behavior of the vizcacha.     

Effects of local extinction of the plains vizcacha (Lagostomus maximus) on vegetation patterns in semi-arid scrub

We studied spatial and temporal effects of local extinction of the plains vizcacha (Lagostomus maximus) on plant communities following widespread, natural extinctions of vizcachas in semi-arid scrub of Argentina. Spatial patterns in vegetation were examined along transects extending outward from active and extinct vizcacha burrow systems. Responses of vegetation to removal of vizcachas were assessed experimentally with exclosures and by documenting vegetation dynamics for 6 years following extinctions. Transect data demonstrated clear spatial patterns in plant cover, particularly an increase in perennial grasses, outward from active vizcacha burrows. These patterns were consistent with predictions based on foraging theory and studies that document grasses as the preferred food of vizcachas. Removal of vizcachas, experimentally and with extinctions, resulted in an immediate increase in perennial and annual forbs indicating that intense herbivory can depress forb cover, as well as grasses. After a 1-year lag following cessation of herbivory, cover of grasses increased. Forbs declined as grasses increased. The long-term effect of extinction of vizcachas was a conversion of colony sites from open patches dominated by forbs to dense bunch grass characteristic of the matrix. Major changes in vegetation occurred within 2–3 years after extinction, resulting in a large pulse of landscape change. However, some species of grasses were uncommon until 5–6 years after the vizcacha extinction. With extinction and colonization, vizcachas generate a dynamic mosaic of patches on the landscape and create temporal, as well as spatial, heterogeneity in semi-arid scrub.     

Phylogeography and demographic history of Shaw's Jird (Meriones shawii complex) in North Africa

Palaeoenvironmental data and climatic reconstructions show that the Mediterranean ecoregion of North Africa underwent drastic ecological changes during the Pleistocene. Given its rich palaeontological record, North Africa is a pertinent region for documenting the role of climate change and human mediated‐habitat changes on the demography and genetic structure of faunal species. In the present study, we collected data from this species in Morocco, Algeria, and Tunisia, and we combined molecular (mitochondrial and nuclear DNA sequences, microsatellites), fossil, palaeoenvironmental, and human context data to propose an explanation for the fluctuations of populations belonging to the Meriones shawii complex in the past. Genetic and fossil data both indicate a strong bottleneck in Moroccan populations at the Middle Holocene (last interglacial optimum) compared to the Late Pleistocene. Our mitochondrial DNA data suggest a diversification event within Morocco corresponding to the 130–125 kya interglacial optimum. Given that (1) major demographic changes in the M. shawii complex coincide with the interglacial optimums, and (2) the impact of human activities on the landscape and faunal communities was moderate during the Middle Holocene (beginnings of the Neolithic culture), our results demonstrate that climate, rather than anthropogenic influences, likely explains the M. shawii complex population decline in the Holocene.     

To what extent do new fossil discoveries change our understanding of clade evolution? A cautionary tale from burying beetles (Coleoptera: Nicrophorus)

Divergence time estimates derived from phylogenies are crucial to infer historical biogeography and diversification dynamics. Yet, the impact of fossil record incompleteness on macroevolutionary reconstructions remains equivocal. Here, we investigate to what extent gaps in the fossil record can impinge downstream evolutionary inferences in the beetle family Silphidae. Recent discoveries have pushed back the fossil record of this group from the Eocene into the Jurassic. We estimated the divergence times of the family using both its currently understood fossil record and the fossil record known prior to these recent discoveries. All fossil calibrations were informed with different parametric distributions to investigate the weight of priors on posterior age estimates. Based on time‐calibrated trees, we assessed the impact of fossil calibrations on the inference of ancestral ranges and diversification rate dynamics in the genus Nicrophorus. Depending upon the selected sets of fossil constraints, the age discrepancies had a major impact on the macroevolutionary inferences: the biogeographic extrapolations relative to paleogeography are markedly contrasting, and the calculated rates at which species form or go extinct (and when they varied) are strikingly different. We show that soft prior distributions do not necessarily alleviate such shortcomings therefore preventing the inference of reliable macroevolutionary patterns in groups presenting a taphonomic bias in their fossil record.     

Mus in Morocco: a Quaternary sequence of intraspecific evolution

North Africa is an intricate biogeographical region at the crossroads of immigration waves from tropical Africa and Asia. Species confined between various barriers (Atlas Mountains, arid environments such as the Sahara in the south, water masses such as the Mediterranean Sea in the north, and the Atlantic Ocean in the west) were generally forced to adapt locally to environmental changes instead of tracking their habitat by shifting their distribution area. The present study aims at providing first insight into the evolution of the genus Mus, and more specifically of the western Mediterranean species Mus spretus in this area. The study relies on the abundant Late Pleistocene and Middle Holocene fossil assemblage from the El Harhoura 2 cave (Rabat‐Témara, Morocco). This exceptional record was studied using geometric morphometrics applied to first upper and lower molars, constituting the most informative and best preserved fossil remains for such small rodents. Two main issues were addressed. (1) Geometric morphometrics was used to clarify taxonomic status and phylogenetic relationships among fossil and modern species in this area. Morphometric analysis revealed good discrimination of most modern and fossil species but failed to document intermediate forms tracing anagenetic evolution. Not mutually exclusive, the occurrence of complex processes of morphological evolution in this genus such as parallel evolution and the action of stabilizing selection may make it difficult to translate patterns of morphological evolution into phylogenetic conclusions. (2) The record was shown to document a sequence of intraspecific evolution of M. spretus. The morphology of the molars through the fossil record of El Harhoura 2 was surprisingly stable despite extensive modern variation. The limited temporal variation largely failed to correlate to palaeoenvironmental proxies. The mouse fossil record at El Harhoura 2 thus presents an intriguing case of morphological stasis despite extensive environmental changes. This long‐term stability may have been recently perturbed by anthropogenic factors including landscape changes and introduction of various competitors and predators, leading to a size reduction. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 599–621.     

Space use of a non-native species,the European hare (<Emphasis Type="Italic">Lepus europaeus</Emphasis>), in habitats of the southern vizcacha (<Emphasis Type="Italic">Lagidium viscacia</Emphasis>) in Northwestern Patagonia,Argentina

Two medium-sized herbivores with high trophic overlap coexist on rocky outcrops in the Patagonian landscape: the southern vizcacha (Lagidium viscacia), which is a native rock specialist, and the European hare (Lepus europaeus), which is a non-native species. We determined the patterns of space use related to distance from outcrops and analyzed spatial overlap between the two species. There were significant differences between the two species in the use of space adjacent to outcrops. The southern vizcacha mainly uses short and medium distances from the outcrop (up to 40 m), whereas the hare’s greatest activity was recorded at distances greater than 50 m. However, there is a partial overlap at medium distances (30–40 m) among both herbivores. Although, in general terms, there is no significant spatial overlap between hares and southern vizcachas, their biological characteristics and the high dietary overlap between the species allow us to predict that, if resources become scarce, the hare could extend its area of activity, as what happens elsewhere, and exploit food resources near outcrops, increasing the vulnerability of vizcacha colonies.     

Locomotory adaptations in entoptychine gophers (Rodentia: Geomyidae) and the mosaic evolution of fossoriality

Pocket gophers (family Geomyidae) are the dominant burrowing rodents in North America today. Their fossil record is also incredibly rich; in particular, entoptychine gophers, a diverse extinct subfamily of the Geomyidae, are known from countless teeth and jaws from Oligocene and Miocene-aged deposits of the western United States and Mexico. Their postcranial remains, however, are much rarer and little studied. Yet, they offer the opportunity to investigate the locomotion of fossil gophers, shed light on the evolution of fossoriality, and enable ecomorphological comparisons with contemporaneous rodents. We present herein a quantitative study of the cranial and postcranial remains of eight different species of entoptychine gophers as well as many contemporary rodent species. We find a range of burrowing capabilities within Entoptychinae, including semifossorial scratch-digging animals and fossorial taxa with cranial adaptations to burrowing. Our results suggest the repeated evolution of chisel-tooth digging across genera. Comparisons between entoptychine gophers and contemporaneous rodent taxa show little ecomorphological overlap and suggest that the succession of burrowing rodent taxa on the landscape may have had more to do with habitat partitioning than competition.     

The impact of the Pull of the Recent on extant elasmobranchs

Modern elasmobranchs have a long evolutionary history and an abundant fossil record that consists mainly of teeth. Many fossil taxa have living representatives. However, the representation of extant taxa in the fossil record is unknown. To begin to understand the geological history of extant elasmobranchs, we here assess the quality of their fossil record. We do so by assessing the Pull of the Recent (POR). The POR can bias the fossil record because the rather complete record of living taxa allows palaeontologists to identify fossil members of the modern clades and to bridge time bins where fossils are absent. We assessed the impact of the POR by quantifying the proportion of extant elasmobranchs that have a fossil record, but do not occur in the last 5 million years (Pliocene and Pleistocene). We found that the POR does not affect orders and families, but it does affect 24% of elasmobranch genera. Within the different elasmobranch orders, the Lamniformes display the most complete generic fossil record, with no impact of the POR. Although modest, the impact of the POR in extant elasmobranch genera is higher than that found in other taxa. Overall, the geological history of elasmobranchs contradicts the usual assumption that the fossil record becomes worse backwards in time. This is the case across geographical regions and tooth size, further suggesting that sampling intensity and outcrop availability might explain the POR effect on sharks and rays.     

The fossil record of extant elasmobranchs

Sharks and their relatives (Elasmobranchii) are highly threatened with extinction due to various anthropogenic pressures. The abundant fossil record of fossil taxa has allowed the tracing of the evolutionary history of modern elasmobranchs to at least 250 MYA; nonetheless, exactly how far back the fossil record of living taxa goes has never been collectively surveyed. In this study, the authors assess the representation and extent of the fossil record of elasmobranchs currently living in our oceans by collecting their oldest records and quantifying first appearance dates at different taxonomic levels (i.e., orders, families, genera and species), ecological traits (e.g., body size, habitat and feeding mechanism) and extinction risks (i.e., threatened, not threatened and data deficient). The results of this study confirm the robust representation of higher taxonomic ranks, with all orders, most of the families and over half of the extant genera having a fossil record. Further, they reveal that 10% of the current global species diversity is represented in the geological past. Sharks are better represented and extend deeper in time than rays and skates. While the fossil record of extant genera (e.g., the six gill sharks, Hexanchus) goes as far back as c. 190 MYA, the fossil record of extant species (e.g., the sand shark, Carcharias taurus Rafinesque 1810) extends c. 66 MYA. Although no significant differences were found in the extent of the fossil record between ecological traits, it was found that the currently threatened species have a significantly older fossil record than the not threatened species. This study demonstrate that the fossil record of extant elasmobranchs extends deep into the geologic time, especially in the case of threatened sharks. As such, the elasmobranch geological history has great potential to advance the understanding of how species currently facing extinction have responded to different stressors in the past, thereby providing a deep-time perspective to conservation.     

Contemporaneous Trace and Body Fossils from a Late Pleistocene Lakebed in Victoria,Australia, Allow Assessment of Bias in the Fossil Record

The co-occurrence of vertebrate trace and body fossils within a single geological formation is rare and the probability of these parallel records being contemporaneous (i.e. on or near the same bedding plane) is extremely low. We report here a late Pleistocene locality from the Victorian Volcanic Plains in south-eastern Australia in which demonstrably contemporaneous, but independently accumulated vertebrate trace and body fossils occur. Bite marks from a variety of taxa are also present on the bones. This site provides a unique opportunity to examine the biases of these divergent fossil records (skeletal, footprints and bite marks) that sampled a single fauna. The skeletal record produced the most complete fauna, with the footprint record indicating a markedly different faunal composition with less diversity and the feeding traces suggesting the presence, amongst others, of a predator not represented by either the skeletal or footprint records. We found that the large extinct marsupial predator Thylacoleo was the only taxon apparently represented by all three records, suggesting that the behavioral characteristics of large carnivores may increase the likelihood of their presence being detected within a fossil fauna. In contrast, Diprotodon (the largest-ever marsupial) was represented only by trace fossils at this site and was absent from the site''s skeletal record, despite its being a common and easily detected presence in late Pleistocene skeletal fossil faunas elsewhere in Australia. Small mammals absent from the footprint record for the site were represented by skeletal fossils and bite marks on bones.     

Molecular and Paleontological Evidence for a Post-Cretaceous Origin of Rodents

The timing of the origin and diversification of rodents remains controversial, due to conflicting results from molecular clocks and paleontological data. The fossil record tends to support an early Cenozoic origin of crown-group rodents. In contrast, most molecular studies place the origin and initial diversification of crown-Rodentia deep in the Cretaceous, although some molecular analyses have recovered estimated divergence times that are more compatible with the fossil record. Here we attempt to resolve this conflict by carrying out a molecular clock investigation based on a nine-gene sequence dataset and a novel set of seven fossil constraints, including two new rodent records (the earliest known representatives of Cardiocraniinae and Dipodinae). Our results indicate that rodents originated around 61.7–62.4 Ma, shortly after the Cretaceous/Paleogene (K/Pg) boundary, and diversified at the intraordinal level around 57.7–58.9 Ma. These estimates are broadly consistent with the paleontological record, but challenge previous molecular studies that place the origin and early diversification of rodents in the Cretaceous. This study demonstrates that, with reliable fossil constraints, the incompatibility between paleontological and molecular estimates of rodent divergence times can be eliminated using currently available tools and genetic markers. Similar conflicts between molecular and paleontological evidence bedevil attempts to establish the origination times of other placental groups. The example of the present study suggests that more reliable fossil calibration points may represent the key to resolving these controversies.     

Predator feeding ecology on Patagonian rocky outcrops: implications for colonies of mountain vizcacha (Lagidium viscacia)

On 10 rocky outcrops with mountain vizcacha colonies, diets and trophic relations of five predator species were analyzed to evaluate their impact in vizcacha populations. Diets included 17 prey items of which mammals represented 97% of biomass. Lagomorphs were the most important prey, followed by sigmodontines, tuco-tucos, and mountain vizcachas. The Barn Owl was a specialized predator, while the culpeo and lesser grison were generalized consumers. Predation of mountain vizcacha by Magellanic Horned Owls and culpeo foxes could increase vizcacha vulnerability because vizcacha populations are small and fragmented, and females produce only one offspring per year.     

Diet selection of the southern vizcacha (<Emphasis Type="Italic">Lagidium viscacia</Emphasis>): a rock specialist in north western Patagonian steppe,Argentina

The southern vizcacha (Lagidium viscacia) is a rock specialist that inhabits small colonies in isolated rocky outcrops of northwestern Patagonia. This study analyzes its diet selection in relation to food availability, establishes the degree of dietary specialization, and discusses the potential competition with exotic herbivores. Diet composition and food availability were determined in summer and winter in eight rocky outcrops by microhistological analysis of fecal pellets, and food availability was estimated by the Braun Blanquet cover abundance scale. Vegetation cover differences were detected by using a random analysis of variance (ANOVA) factorial block design, and dietary preferences were determined by the confidence interval of Bonferroni. The southern vizcacha showed a specialized feeding behavior despite the consumption of a wide variety of items. Their diet was concentrated on a few types of food, mainly grasses, and the trophic niche was narrow and without seasonal variations. In winter, when food was scarce and of lower quality than summer, diet was dominated by Stipa speciosa, suggesting a selection according to the selective quality hypothesis. Our results (narrow trophic niche, restricted activity near rocky outcrops, and a diet with high proportions of low-quality grasses) showed that the vizcacha is an obligatory dietary specialist, and these characteristics made it highly vulnerable to changes in food availability. In this scenario, overgrazing caused by alien species with similar diets, as the European hare and livestock, could negatively affect their colonies.     

A comment on the earliest spalacinae (rodentia,Muroidea)

According to F. M. Catzefliset al. (Trends Ecol. Evol. 7, 122–126, 1992), comparative dating of the oldest dichotomy in the muroid group (Spalacinae-other Muridae) by molecular and paleontological time scales produces conflicting results. For the earliest Spalacinae they refer to a date of 25–37 Ma; however, it has been demonstrated thatRhizospalax is not a muroid rodent, and a review of the record of fossil Spalacinae suggests that paleontological and molecular dating produces a comparable age (±19 Ma).     

Enamel Microstructure of Rodent Molars, Classification, and Parallelisms, with a Note on the Systematic Affiliation of the Enigmatic Eocene Rodent Protoptychus

To investigate the diversity of the enamel structures in rodent molars, the schmelzmuster of more than 270 genera from the various fossil and extant groups was investigated. Only three basic types of schmelzmuster were recognized. The most prominent one, the C-type, is characterized by a basal ring of lamellar enamel (BRLE) surrounding the molars at the base of the crown. It occurs in most murids (cricetids) and other Myodonta. It is shared by the Dipodidea, Eomyidae, Geomyidae, and Gliridae. The C-type schmelzmuster was not found in any of the other rodents groups (Sciuromorpha, Anomaluromorpha, Sciuravida, Hystricognathi, Bathyergomorphi, and Caviida). Despite the rare occurrence of the P-type schmelzmuster with radial enamel only, most of these rodents have thick Hunter–Schreger bands (HSB) in their molars (S-type schmelzmuster). Although the C-type schmelzmuster is strictly limited to the Myomorpha (sensu McKenna and Bell), the fossil record shows that this structure does not form a synapomorphy but developed in parallel mostly from the P-type, but in Gliridae from the S-type schmelzmuster. On the basis of molar and incisor enamel the systematic position of Protoptychus can be evaluated.     

The bite force of the largest fossil rodent (Hystricognathi,Caviomorpha, Dinomyidae)

Blanco R.E., Rinderknecht, A. & Lecuona, G. 2011: The bite force of the largest fossil rodent (Hystricognathi, Caviomorpha, Dinomyidae). Lethaia, Vol. 45, pp. 157–163. An exceptionally well‐preserved skull of the largest fossil rodent Josephoartigasia monesi allows the first analysis of the bite mechanics of this group of South American giant rodents. In this study, we reconstructed the main anatomical features of the skull of this Pliocene rodent, relating them to the bite force at incisors. Bite force was estimated using three different techniques. Two methods suggest that bite forces at incisors of around 1000 N were possible for these mammals. However, the incisors seem to be stronger than expected for this bite force implying that the bite forces may have been greater than 3000 N. We consider three hypotheses: allometric effects, teeth digging or defence against predators, to explain our results. □Bite force, Dinomyidae, incisors, largest rodent, Pliocene.     

Evaluation of the fossil fish‐specific diversity in a chadian continental assemblage: Exploration of morphological continuous variation in Synodontis (Ostariophysi,Siluriformes)

In the fossil record, the quantification of continuous morphological variation has become a central issue when dealing with species identification and speciation. In this context, fossil taxa with living representatives hold great promise, because of the potential to characterise patterns of intraspecific morphological variation in extant species prior to any interpretation in the fossil record. The vast majority of catfish families fulfil this prerequisite, as most of them are represented by extant genera. However, although they constitute a major fish group in terms of distribution, and ecological and taxonomic diversity, the quantitative study of their past morphological variation has been neglected, as fossil specimens are generally identified based on the scarcest remains, that is, complete neurocrania that bear discrete characters. Consequently, a part of freshwater catfish history is unprospected and unknown. In this study, we explored the morphological continuous variation of the humeral plate shape in Synodontis catfishes using Elliptic Fourier Analysis (EFA), and compared extant members and fossil counterparts. We analysed 153 extant specimens of 11 Synodontis species present in the Chad basin, in addition to 23 fossil specimens from the Chadian fossiliferous area of Toros Menalla which is dated around 7 Ma. This highly speciose genus, which is one of the most diversified in Africa, exhibits a rich fossil record with several hundred remains mostly identified as Synodontis sp. The analysis of the outline of the humeral plate reveals that some living morphological types were already represented in the Chad Basin 7 My ago, and allows for the discovery of extinct species. Beside illuminating the complex Neogene evolutionary history of Synodontis, these results underline the interest in the ability of isolated remains to reconstruct a past dynamic history and to validate the relevance of EFA as a tool to explore specific diversity through time. J. Morphol. 277:1486–1496, 2016. © 2016 Wiley Periodicals, Inc.     

Contrasting patterns of disparity suggest differing constraints on the evolution of trilobite cephalic structures during the Cambrian ‘explosion’

Trilobites are an abundant group of Palaeozoic marine euarthropods that appear abruptly in the fossil record c. 521 million years ago. Quantifying the development of morphological variation (or ‘disparity’) through time in fossil groups like trilobites is critical in understanding evolutionary radiations such as the Cambrian ‘explosion’. Here, I use geometric morphometrics to quantify ‘cumulative disparity’ in functionally-important structures within the trilobite cephalon across their initial radiation during Cambrian Series 2. Overall cephalic disparity increased rapidly and attained a maximum within several million years. This pattern is dominated by the cephalic outline (in particular the genal spines), reflecting rapid, convergent expansion to the extremes of morphospace in a few early families. In contrast, removing the outline and focusing on structures such as the glabella and eye ridges (associated with feeding and vision, respectively) showed a more gradual increase in disparity, closer in line with taxonomic diversity and supporting the hypothesis of a relatively accurate trilobite fossil record. These contrasting patterns suggest that disparity in different structures was constrained in different ways, with extrinsic (ecological) factors probably having the major impact on overall disparity. It also implies that patterns of disparity in isolated substructures cannot necessarily be taken individually as representative of overall morphologies.