Combined data analysis of fossil and living mammals: a Paleogene sister taxon of Placentalia and the antiquity of Marsupialia.

The Cretaceous-Paleogene (KPg) boundary, one of Earth's five major extinction events, occurred just before the appearance of Placentalia in the fossil record. The Gobi Desert, Mongolia and the Western Interior of North America have important fossil mammals occurring just before and after the KPg boundary (e.g. Prodiacodon, Deltatheridium) that have yet to be phylogenetically tested in a character-rich context with molecular data. We present here phylogenetic analyses of >6000 newly scored anatomical observations drawn from six untested fossils and added to the largest existing morphological matrix for mammals. These data are combined with sequence data from 27 nuclear genes. Results show the existence of a new eutherian sister clade to Placentalia, which we name and characterize. The extinct clade Leptictidae is part of this placental sister clade, indicating that the sister clade survived the KPg event to co-exist in ancient ecosystems during the Paleogene radiation of placentals. Analysing the Cretaceous metatherian Deltatheridium in this character-rich context reveals it is a member of Marsupialia, a finding that extends the minimum age of Marsupialia before the KPg boundary. Numerous shared-derived features from multiple anatomical systems support the assignment of Deltatheridium to Marsupialia. Computed tomography scans of exquisite new specimens better document the marsupial-like dental replacement pattern of Deltatheridium. The new placental sister clade has both Asian and North American species, and is ancestrally characterized by shared derived features such as a hind limb modified for saltatorial locomotion.

The role and impact of Zootaxa in mammalogy in its first 20 years.

Zootaxa came as a new and innovative publication medium for taxonomy, amidst a scenario of devaluation of this important biological science. After 20 years, it has ascertained itself as one of the main journals in animal taxonomy. However, the contribution of the journal to the taxonomy of Mammalia (mammals), one of the most studied groups of animals with a long-standing, dedicated spectrum of specialized journals (mammalogy), could have been expected as minor. All the current and former editors of the Mammalia section of Zootaxa analyzed the relative contribution of the journal to the description of new species of mammals since 2001. We also analyzed the contribution of Zootaxa by taxon, geographic origin of taxa, and geographic origin of first authors. The taxonomic methodology of authors in species description is described as well as the temporal trends in publications and publication subjects. We highlight the editors' picks and eventually, the challenges for the future. We found that Zootaxa has had a significant contribution to mammalogy, being the second journal (the first being Journal of Mammalogy) in terms of number of new species described (76; 10.6% of the new mammalian species described between 2001 and 2020). The majority of the new species were described following an integrative taxonomic approach with at least two sources of data (86%). The analysis of published taxa, their geographic origin, and the country of origin of first authors shows a wide coverage and exhaustive representation, except for the species from the Nearctic. We conclude that Zootaxa has likely responded to a repressed demand for an additional taxonomic journal in mammalogy, with as possible appeals the absence of publication fees and an established publication speed. With 246 articles published in the past 20 years, the Mammalia section of Zootaxa embraces a large spectrum of systematic subjects going beyond alpha taxonomy. The challenges for the future are to encourage publications of authors from the African continent, still poorly represented, and from the palaeontology community, as the journal has been open to palaeontology since its early days.

Systematics and Taxonomy of Tonatia saurophila Koopman & Williams, 1951 (Chiroptera, Phyllostomidae).

The Stripe-headed Round-eared bat, Tonatia saurophila, includes three subspecies: Tonatia saurophila saurophila (known only from subfossil records in Jamaica), Tonatia saurophila bakeri (distributed from southeastern Mexico to northern Colombia, Venezuela west and north of the Cordillera de Mérida, and northwestern Ecuador), and Tonatia saurophila maresi (distributed in Venezuela east and south of the Cordillera de Mérida, the Guianas, Trinidad and Tobago, northeastern Brazil, and along the upper Amazon basin in Colombia, Ecuador, Peru, and Bolivia). The last two subspecies are an attractive example to test predictions about the historical role of the Andes in mammalian diversification. Based on morphological descriptions, morphometric analyses, and phylogenetic reconstruction using the mitochondrial gene Cyt-b and the nuclear exon RAG2, this study evaluates the intraspecific relationships within Tonatia saurophila and the taxonomic status of the taxon. The three subspecies of T. saurophila are recognizable as full species: Tonatia bakeri, Tonatia maresi, and Tonatia saurophila. The latter is restricted to its type locality and possibly is extinct. Tonatia bakeri, in addition to being larger than T. maresi, is morphologically distinguishable by possessing an acute apex at the posterior edge of the skull, a well-developed clinoid process, and relatively robust mandibular condyles, and by lacking a diastema between the canine and the first lower premolar. The genetic distance between T. bakeri and T. maresi is 7.65%.

ResumenEl Murciélago de orejas redondas de cabeza rayada, Tonatia saurophila, incluye tres subespecies: Tonatia saurophila saurophila (conocida sólo por registros subfósiles en Jamaica), Tonatia saurophila bakeri (distribuida desde el sureste de México hasta el norte de Colombia, Venezuela al oeste y norte de la Cordillera de Mérida, y el noroeste de Ecuador), y Tonatia saurophila maresi (distribuida en Venezuela al este y sur de la Cordillera de Mérida, las Guayanas, Trinidad y Tobago, el noreste de Brasil, y la vertiente amazónica de los Andes de Colombia, Ecuador, Peru y Bolivia). Las dos últimas subespecies representan un ejemplo atractivo para poner a prueba predicciones sobre el rol histórico de los Andes en la diversificación de mamíferos. Con base en descripciones morfológicas, análisis morfométricos y una reconstrucción filogenética empleando el gen mitocondrial Cyt-b y el gen nuclear RAG2, este estudio evalúa las relaciones intraspecíficas dentro de Tonatia saurophila y el estatus taxonómico del taxón. Las tres subespecies de T. saurophila son reconocidas como especies plenas: Tonatia bakeri, T. maresi y T. saurophila. Esta última está restringida a la localidad tipo y posiblemente está extinta. Tonatia bakeri, además de ser de mayor tamaño que T. maresi, se diferencia morfológicamente por poseer un ápice agudo en el borde posterior del cráneo, un proceso clinoideo bien desarrollado y cóndilos mandibulares relativamente robustos, y por carecer de un diastema entre el canino y el primer premolar inferior. La distancia genética entre T. bakeri y T. maresi es 7.65%.

Crowds Replicate Performance of Scientific Experts Scoring Phylogenetic Matrices of Phenotypes.

Scientists building the Tree of Life face an overwhelming challenge to categorize phenotypes (e.g., anatomy, physiology) from millions of living and fossil species. This biodiversity challenge far outstrips the capacities of trained scientific experts. Here we explore whether crowdsourcing can be used to collect matrix data on a large scale with the participation of nonexpert students, or "citizen scientists." Crowdsourcing, or data collection by nonexperts, frequently via the internet, has enabled scientists to tackle some large-scale data collection challenges too massive for individuals or scientific teams alone. The quality of work by nonexpert crowds is, however, often questioned and little data have been collected on how such crowds perform on complex tasks such as phylogenetic character coding. We studied a crowd of over 600 nonexperts and found that they could use images to identify anatomical similarity (hypotheses of homology) with an average accuracy of 82% compared with scores provided by experts in the field. This performance pattern held across the Tree of Life, from protists to vertebrates. We introduce a procedure that predicts the difficulty of each character and that can be used to assign harder characters to experts and easier characters to a nonexpert crowd for scoring. We test this procedure in a controlled experiment comparing crowd scores to those of experts and show that crowds can produce matrices with over 90% of cells scored correctly while reducing the number of cells to be scored by experts by 50%. Preparation time, including image collection and processing, for a crowdsourcing experiment is significant, and does not currently save time of scientific experts overall. However, if innovations in automation or robotics can reduce such effort, then large-scale implementation of our method could greatly increase the collective scientific knowledge of species phenotypes for phylogenetic tree building. For the field of crowdsourcing, we provide a rare study with ground truth, or an experimental control that many studies lack, and contribute new methods on how to coordinate the work of experts and nonexperts. We show that there are important instances in which crowd consensus is not a good proxy for correctness.

Bayesian hierarchical models suggest oldest known plant-visiting bat was omnivorous.

The earliest record of plant visiting in bats dates to the Middle Miocene of La Venta, the world's most diverse tropical palaeocommunity. Palynephyllum antimaster is known from molars that indicate nectarivory. Skull length, an important indicator of key traits such as body size, bite force and trophic specialization, remains unknown. We developed Bayesian models to infer skull length based on dental measurements. These models account for variation within and between species, variation between clades, and phylogenetic error structure. Models relating skull length to trophic level for nectarivorous bats were then used to infer the diet of the fossil. The skull length estimate for Palynephyllum places it among the larger lonchophylline bats. The inferred diet suggests Palynephyllum fed on nectar and insects, similar to its living relatives. Omnivory has persisted since the mid-Miocene. This is the first study to corroborate with fossil data that highly specialized nectarivory in bats requires an omnivorous transition.

A new species of broad-nosed bat Platyrrhinus Saussure, 1860 (Chiroptera: Phyllostomidae) from the Guianan Shield.

A new species of broad-nosed bat Platyrrhinus Saussure, 1860 (Chiroptera: Phyllostomidae: Stenodermatinae) from the Guianan Shield is described based on molecular and morphological data. Previously confused with P. helleri and P. recifinus, the new taxon is currently known from only Guyana and Suriname and is most closely related to P. recifinus from eastern Brazil and not to the two sympatric species (P. fusciventris and P. incarum) also recently recognized as distinct from P. helleri. Morphometrically the new taxon overlaps with the smaller species of the genus (P. angustirostris, P. brachycephalus, P. fusciventris, P. helleri, P. incarum, and P. matapalensis), but forms a different cluster from the larger P. recifinus. Morphologically the new taxon is distinguished from its congeners by a combination of external and craniodental characteristics. Platyrrhinus now includes 21 species making it the most speciose genus in the Neotropical family Phyllostomidae.

Two new species of yellow-shouldered bats, genus Sturnira Gray, 1842 (Chiroptera, Phyllostomidae) from Costa Rica, Panama and western Ecuador.

Two new species of yellow-shouldered bats Sturnira Gray, 1842 (Chiroptera, Phyllostomidae) from Central America and western South America are described using molecular and morphological data. The two new species, which occur in Costa Rica and Panama and in western Ecuador, were previously confused with S. ludovici, and S. lilium and S. luisi, respectively. Sturnira now includes 22 described species, making it the most speciose genus in the Neotropical family Phyllostomidae.

Integrating incomplete fossils by isolating conflicting signal in saturated and non-independent morphological characters.

Morphological characters are indispensable in phylogenetic analyses for understanding the pattern, process, and tempo of evolution. If characters are independent and free of systematic errors, then combining as many different kinds of characters as are available will result in the best-supported phylogenetic hypotheses. But since morphological characters are subject to natural selection for function and arise from the expression of developmental pathways, they may not be independent, a situation that may amplify any underlying homoplasy. Here, we use new dental and multi-locus genetic data from bats (Mammalia: Chiroptera) to quantify saturation and similarity in morphological characters and introduce two likelihood-based approaches to identify strongly conflicting characters and integrate morphological and molecular data. We implement these methods to analyze the phylogeny of incomplete Miocene fossils in the radiation of Phyllostomidae (New World Leaf-nosed Bats), perhaps the most ecologically diverse family of living mammals. Morphological characters produced trees incongruent with molecular phylogenies, were saturated, and showed rates of change higher than most molecular substitution rates. Dental characters encoded variation similar to that in other morphological characters, while molecular characters encoded highly dissimilar variation in comparison. Saturation and high rates of change indicate randomization of phylogenetic signal in the morphological data, and extensive similarity suggests characters are non-independent and errors are amplified. To integrate the morphological data into tree building while accounting for homoplasy, we used statistical molecular scaffolds and combined phylogenetic analyses excluding a small subset of strongly conflicting dental characters. The phylogenies revealed the Miocene nectar-feeding †Palynephyllum nests within the crown nectar-feeding South American subfamily Lonchophyllinae, while the Miocene genus †Notonycteris is sister to the extant carnivorous Vampyrum. These relationships imply new calibration points for timing of radiation of the ecologically diverse Phyllostomidae. [Chiroptera; conflict; dentition; morphology; Phyllostomidae; saturation; scaffold; systematic error.].

Transitions between Andean and Amazonian centers of endemism in the radiation of some arboreal rodents.

BACKGROUND: The tropical Andes and Amazon are among the richest regions of endemism for mammals, and each has given rise to extensive in situ radiations. Various animal lineages have radiated ex situ after colonizing one of these regions from the other: Amazonian clades of dendrobatid frogs and passerine birds may have Andean ancestry, and transitions from the Amazon to Andes may be even more common. To examine biogeographic transitions between these regions, we investigated the evolutionary history of three clades of rodents in the family Echimyidae: bamboo rats (Dactylomys-Olallamys-Kannabateomys), spiny tree-rats (Mesomys-Lonchothrix), and brush-tailed rats (Isothrix). Each clade is distributed in both the Andes and Amazonia, and is more diverse in the lowlands. We used two mitochondrial (cyt-b and 12S) and three nuclear (GHR, vWF, and RAG1) markers to reconstruct their phylogenetic relationships. Tree topologies and ancestral geographic ranges were then used to determine whether Andean forms were basal to or derived from lowland radiations. RESULTS: Four biogeographic transitions are identified among the generic radiations. The bamboo rat clade unambiguously originated in the Amazon ca. 9 Ma, followed by either one early transition to the Andes (Olallamys) and a later move to the Amazon (Dactylomys), or two later shifts to the Andes (one in each genus). The Andean species of both Dactylomys and Isothrix are sister to their lowland species, raising the possibility that highland forms colonized the Amazon Basin. However, uncertainty in their reconstructed ancestral ranges obscures the origin of these transitions. The lone Andean species of Mesomys is confidently nested within the lowland radiation, thereby indicating an Amazon-to-Andes transition ca. 2 Ma. CONCLUSIONS: Differences in the timing of these biogeographic transitions do not appear to explain the different polarities of these trees. Instead, even within the radiation of a single family, both Andean and Amazonian centers of endemism appear enriched by lineages that originated in the other region. Our survey of other South American lineages suggests a pattern of reciprocal exchange between these regions-among mammals, birds, amphibians, and insects we found no fewer than 87 transitions between the Andes and Amazon from Miocene-Pleistocene. Because no clear trend emerges between the timing and polarity of transitions, or in their relative frequency, we suggest that reciprocal exchange between tropical highland and lowland faunas in South America has been a continual process since ca. 12 Ma.

Response to comment on "The placental mammal ancestor and the post-K-Pg radiation of placentals".

Tree-building with diverse data maximizes explanatory power. Application of molecular clock models to ancient speciation events risks a bias against detection of fast radiations subsequent to the Cretaceous-Paleogene (K-Pg) event. Contrary to Springer et al., post-K-Pg placental diversification does not require "virus-like" substitution rates. Even constraining clade ages to their model, the explosive model best explains placental evolution.

Next-generation phenomics for the Tree of Life.

The phenotype represents a critical interface between the genome and the environment in which organisms live and evolve. Phenotypic characters also are a rich source of biodiversity data for tree building, and they enable scientists to reconstruct the evolutionary history of organisms, including most fossil taxa, for which genetic data are unavailable. Therefore, phenotypic data are necessary for building a comprehensive Tree of Life. In contrast to recent advances in molecular sequencing, which has become faster and cheaper through recent technological advances, phenotypic data collection remains often prohibitively slow and expensive. The next-generation phenomics project is a collaborative, multidisciplinary effort to leverage advances in image analysis, crowdsourcing, and natural language processing to develop and implement novel approaches for discovering and scoring the phenome, the collection of phentotypic characters for a species. This research represents a new approach to data collection that has the potential to transform phylogenetics research and to enable rapid advances in constructing the Tree of Life. Our goal is to assemble large phenomic datasets built using new methods and to provide the public and scientific community with tools for phenomic data assembly that will enable rapid and automated study of phenotypes across the Tree of Life.

Diversification of the yellow-shouldered bats, genus Sturnira (Chiroptera, Phyllostomidae), in the New World tropics.

The Yellow-shouldered bats, Genus Sturnira, are widespread, diverse, and abundant throughout the Neotropical Region, but little is known of their phylogeny and biogeography. We collected 4409 bp of DNA from three mitochondrial (cyt-b, ND2, D-loop) and two nuclear (RAG1, RAG2) sequences from 138 individuals representing all but two recognized species of Sturnira and five other phyllostomid bats used as outgroups. The sequence data were subjected to maximum parsimony, maximum likelihood, and Bayesian inference analyses. Results overwhelmingly support the monophyly of the genus Sturnira but not continued recognition of Corvira as a subgenus; the two species (bidens and nana) allocated to that group constitute separate, basal branches on the phylogeny. A total of 21 monophyletic putatively species-level groups were recovered; pairs were separated by an average 7.09% (SD=1.61) pairwise genetic distance in cyt-b, and three of these groups are apparently unnamed. Several well-supported clades are evident, including a complex of seven species formerly confused with S. lilium, a species that is actually limited to the Brazilian Shield. We used four calibration points to construct a time-tree for Sturnira, using BEAST. Sturnira diverged from other stenodermatines in the mid-Miocene, and by the end of that epoch (5.3 Ma), three basal lineages were present. Most living species belong to one of two clades, A and B, which appeared and diversified shortly afterwards, during the Pliocene. Both parsimony (DIVA) and likelihood (Lagrange) methods for reconstructing ancestral ranges indicate that the radiation of Sturnira is rooted in the Andes; all three basal lineages (in order, bidens, nana, and aratathomasi) have strictly or mainly Andean distributions. Only later did Sturnira colonize the Pacific lowlands (Chocó) and thence Central America. Sturnira species that are endemic to Central America appeared after the final emergence of the Panamanian landbridge ~3 Ma. Despite its ability to fly and to colonize the Antilles overwater, this genus probably accompanied the "legions" of South American taxa that moved overland during the Great American Biotic Interchange. Its eventual colonization of the Lesser Antilles and the appearance of two endemic lineages there did not take place until the Pleistocene. Because of its continual residence and diversification in South America, Andean assemblages of Sturnira contain both basal and highly derived members of the genus.

The placental mammal ancestor and the post-K-Pg radiation of placentals.

To discover interordinal relationships of living and fossil placental mammals and the time of origin of placentals relative to the Cretaceous-Paleogene (K-Pg) boundary, we scored 4541 phenomic characters de novo for 86 fossil and living species. Combining these data with molecular sequences, we obtained a phylogenetic tree that, when calibrated with fossils, shows that crown clade Placentalia and placental orders originated after the K-Pg boundary. Many nodes discovered using molecular data are upheld, but phenomic signals overturn molecular signals to show Sundatheria (Dermoptera + Scandentia) as the sister taxon of Primates, a close link between Proboscidea (elephants) and Sirenia (sea cows), and the monophyly of echolocating Chiroptera (bats). Our tree suggests that Placentalia first split into Xenarthra and Epitheria; extinct New World species are the oldest members of Afrotheria.

Laelapinae mites (Acari: Parasitiformes: Laelapidae) parasitic of sigmodontine rodents from northern Peru, with the description of a new species from Akodon aerosus (Rodentia: Cricetidae: Sigmodontinae).

Laelapine mites are common parasites of sigmodontine rodents in the Neotropics. However, few species are reported from Peru as a result of the low number of mammal surveys that include ectoparasite collections. Herein we report 12 species of mites from northern Peru. From these, 8 are reported for the first time for the country, and 1 is new to science , Androlaepaps aerosus sp. nov., the latter associated exclusively with the sigmodontine Akodon aerosus . Most of the laelapine species were host specific. The new species, included in the Androlaelaps rotundus species group, resembles An. rotundus "sensu stricto" and An. ulysespardinasi in general appearance but is unique in the length of the hypostomal seta h3 (>58 µm), which is 3 times as long as the gnathosomal seta, and its tip reaching or over-reaching the gnathosomal setal bases; dorsal seta j2 is very long (>70 µm), almost reaching the point of j3.

Phylogenetics and biogeography of the broad-nosed bats, genus Platyrrhinus (Chiroptera: Phyllostomidae).

The Neotropical broad-nosed bats, genus Platyrrhinus, represent a well-defined monophyletic group of 14 recognized species. A recent study of morphological characters confirmed Platyrrhinus monophyly and species diagnosis, but offered little support to their intra-specific relationships. We conducted phylogenetic analyses of the genus, using dense taxonomic sampling in combination with four gene sequences representing both mitochondrial and nuclear DNA transmission systems. Our aim was to elucidate the phylogenetic structure among species, using the resulting 3341 bp of DNA. Maximum parsimony, maximum likelihood, and Bayesian inference analyses produced similar topologies that confirm the monophyly of the genus Platyrrhinus and strongly support many previously unrecognized groups. Paraphyly of Platyrrhinus helleri and the unclear position of P. brachycephalus in the clades were also apparent in the data. Our biogeographical analysis suggests a Brazilian Shield origin for Platyrrhinus, followed by subsequent radiations of lineages in the Amazon Basin and Andes. Secondary dispersal from Amazonian and Andean centers is responsible for the Platyrrhinus inhabiting the Guianan Shield and the Pacific lowlands and Central America, respectively.

A framework for assessment and monitoring of small mammals in a lowland tropical forest.

Development projects in tropical forests can impact biodiversity. Assessment and monitoring programs based on the principles of adaptive management assist managers to identify and reduce such impacts. The small mammal community is one important component of a forest ecosystem that may be impacted by development projects. In 1996, a natural gas exploration project was initiated in a Peruvian rainforest. The Smithsonian Institution's Monitoring and Assessment of Biodiversity program cooperated with Shell Prospecting and Development Peru to establish an adaptive management program to protect the region's biodiversity. In this article, we discuss the role of assessing and monitoring small mammals in relation to the natural gas project. We outline the conceptual issues involved in establishing an assessment and monitoring program, including setting objectives, evaluating the results and making appropriate decisions. We also summarize the steps taken to implement the small mammal assessment, provide results from the assessment and discuss protocols to identify appropriate species for monitoring.