Evolutionary History of Lagomorphs in Response to Global Environmental Change

Although species within Lagomorpha are derived from a common ancestor, the distribution range and body size of its two extant groups, ochotonids and leporids, are quite differentiated. It is unclear what has driven their disparate evolutionary history. In this study, we compile and update all fossil records of Lagomorpha for the first time, to trace the evolutionary processes and infer their evolutionary history using mitochondrial genes, body length and distribution of extant species. We also compare the forage selection of extant species, which offers an insight into their future prospects. The earliest lagomorphs originated in Asia and later diversified in different continents. Within ochotonids, more than 20 genera occupied the period from the early Miocene to middle Miocene, whereas most of them became extinct during the transition from the Miocene to Pliocene. The peak diversity of the leporids occurred during the Miocene to Pliocene transition, while their diversity dramatically decreased in the late Quaternary. Mantel tests identified a positive correlation between body length and phylogenetic distance of lagomorphs. The body length of extant ochotonids shows a normal distribution, while the body length of extant leporids displays a non-normal pattern. We also find that the forage selection of extant pikas features a strong preference for C₃ plants, while for the diet of leporids, more than 16% of plant species are identified as C₄ (31% species are from Poaceae). The ability of several leporid species to consume C₄ plants is likely to result in their size increase and range expansion, most notably in Lepus. Expansion of C₄ plants in the late Miocene, the so-called ‘nature’s green revolution’, induced by global environmental change, is suggested to be one of the major ‘ecological opportunities’, which probably drove large-scale extinction and range contraction of ochotonids, but inversely promoted diversification and range expansion of leporids.     

When parasites persist: tapeworms survive host extinction and reveal waves of dispersal across Beringia

Investigations of intercontinental dispersal between Asia and North America reveal complex patterns of geographic expansion, retraction and isolation, yet historical reconstructions are largely limited by the depth of the record that is retained in patterns of extant diversity. Parasites offer a tool for recovering deep historical insights about the biosphere, improving the resolution of past community-level interactions. We explored biogeographic hypotheses regarding the history of dispersal across Beringia, the region intermittently linking Asia and North America, through large-scale multi-locus phylogenetic analyses of the genus Schizorchis, an assemblage of host-specific cestodes in pikas (Lagomorpha: Ochotonidae). Our genetic data support palaeontological evidence for two separate geographic expansions into North America by Ochotona in the late Tertiary, a history that genomic evidence from extant pikas does not record. Pikas descending from the first colonization of Miocene age persisted into the Pliocene, subsequently coming into contact with a second wave of Nearctic colonists from Eurasia before going extinct. Spatial and temporal overlap of historically independent pika populations provided a window for host colonization, allowing persistence of an early parasite lineage in the contemporary fauna following the extinction of its ancestral hosts. Empirical evidence for ancient ‘ghost assemblages'' of hosts and parasites demonstrates how complex mosaic faunas are assembled in the biosphere through episodes of faunal mixing encompassing parasite lineages across deep and shallow time.     

Oryctolagus giberti n. sp. (Lagomorpha, Mammalia) du Pléistocène inférieur de Cueva Victoria (Murcie, Espagne)

A new species of leporid (Lagomorpha, Mammalia) is described based on the material from the Lower Pleistocene of Cueva Victoria (Murcia, Spain). This species, named Oryctolagus giberti n. sp., presents several intermediate characters between the first known representative of the genus, O. laynensis, from the Middle Pliocene of Spain, and the modern European rabbit (O. cuniculus), specially at the level of the palate, the mandible, the third lower premolar, the ulna, the coxal and the femur. In this respect, Oryctolagus giberti n. sp. is a firm candidate to occupy the vacant phylogenetic place between these two species. It also questions the results of molecular studies that date the divergence of groups A and B of Oryctolagus cuniculus at about 2 Myr ago.     

A morphometric mapping analysis of lower fourth deciduous premolar in hominoids: Implications for phylogenetic relationship between Nakalipithecus and Ouranopithecus

Clarifying morphological variation among African and Eurasian hominoids during the Miocene is of particular importance for inferring the evolutionary history of humans and great apes. Among Miocene hominoids, Nakalipithecus and Ouranopithecus play an important role because of their similar dates on different continents. Here, we quantify the lower fourth deciduous premolar (dp4) inner morphology of extant and extinct hominoids using a method of morphometric mapping and examine the phylogenetic relationships between these two fossil taxa. Our data indicate that early Late Miocene apes represent a primitive state in general, whereas modern great apes and humans represent derived states. While Nakalipithecus and Ouranopithecus show similarity in dp4 morphology to a certain degree, the dp4 of Nakalipithecus retains primitive features and that of Ouranopithecus exhibits derived features. Phenotypic continuity among African ape fossils from Miocene to Plio-Pleistocene would support the African origin of African apes and humans (AAH). The results also suggest that Nakalipithecus could have belonged to a lineage from which the lineage of Ouranopithecus and the common ancestor of AAH subsequently derived.     

Faster Speciation and Reduced Extinction in the Tropics Contribute to the Mammalian Latitudinal Diversity Gradient

The increase in species richness from the poles to the tropics, referred to as the latitudinal diversity gradient, is one of the most ubiquitous biodiversity patterns in the natural world. Although understanding how rates of speciation and extinction vary with latitude is central to explaining this pattern, such analyses have been impeded by the difficulty of estimating diversification rates associated with specific geographic locations. Here, we use a powerful phylogenetic approach and a nearly complete phylogeny of mammals to estimate speciation, extinction, and dispersal rates associated with the tropical and temperate biomes. Overall, speciation rates are higher, and extinction rates lower, in the tropics than in temperate regions. The diversity of the eight most species-rich mammalian orders (covering 92% of all mammals) peaks in the tropics, except that of the Lagomorpha (hares, rabbits, and pikas) reaching a maxima in northern-temperate regions. Latitudinal patterns in diversification rates are strikingly consistent with these diversity patterns, with peaks in species richness associated with low extinction rates (Primates and Lagomorpha), high speciation rates (Diprotodontia, Artiodactyla, and Soricomorpha), or both (Chiroptera and Rodentia). Rates of range expansion were typically higher from the tropics to the temperate regions than in the other direction, supporting the “out of the tropics” hypothesis whereby species originate in the tropics and disperse into higher latitudes. Overall, these results suggest that differences in diversification rates have played a major role in shaping the modern latitudinal diversity gradient in mammals, and illustrate the usefulness of recently developed phylogenetic approaches for understanding this famous yet mysterious pattern.     

Phylogenetic relationships and infrageneric classification of Epidendrum subgenus Amphiglottium (Laeliinae, Orchidaceae)

Epidendrum L. is the largest genus of Orchidaceae in the Neotropical region; it has an impressive morphological diversification, which imposes difficulties in delimitation of both infrageneric and interspecific boundaries. In this study, we review infrageneric boundaries within the subgenus Amphiglottium and try to contribute to the understanding of morphological diversification and taxa delimitation within this group. We tested the monophyly of the subgenus Amphiglottium sect. Amphiglottium, expanding previous phylogenetic investigations and reevaluated previous infrageneric classifications proposed. Sequence data from the trnL-trnF region were analyzed with both parsimony and maximum likelihood criteria. AFLP markers were also obtained and analyzed with phylogenetic and principal coordinate analyses. Additionally, we obtained chromosome numbers for representative species within the group. The results strengthen the monophyly of the subgenus Amphiglottium but do not support the current classification system proposed by previous authors. Only section Tuberculata comprises a well-supported monophyletic group, with sections Carinata and Integra not supported. Instead of morphology, biogeographical and ecological patterns are reflected in the phylogenetic signal in this group. This study also confirms the large variability of chromosome numbers for the subgenus Amphiglottium (numbers ranging from 2n = 24 to 2n = 240), suggesting that polyploidy and hybridization are probably important mechanisms of speciation within the group.     

Comparison between Colony Morphology and Molecular Phylogeny in the Caribbean Scleractinian Coral Genus Madracis

A major challenge in coral biology is to find the most adequate and phylogenetically informative characters that allow for distinction of closely related coral species. Therefore, data on corallite morphology and genetic data are often combined to increase phylogenetic resolution. In this study, we address the question to which degree genetic data and quantitative information on overall coral colony morphologies identify similar groupings within closely related morphospecies of the Caribbean coral genus Madracis. Such comparison of phylogenies based on colony morphology and genetic data will also provide insight into the degree to which genotype and phenotype overlap. We have measured morphological features of three closely related Caribbean coral species of the genus Madracis (M. formosa, M. decactis and M. carmabi). Morphological differences were then compared with phylogenies of the same species based on two nuclear DNA markers, i.e. ATPSα and SRP54. Our analysis showed that phylogenetic trees based on (macroscopical) morphological properties and phylogenetic trees based on DNA markers ATPSα and SRP54 are partially similar indicating that morphological characteristics at the colony level provide another axis, in addition to commonly used features such as corallite morphology and ecological information, to delineate genetically different coral species. We discuss this new method that allows systematic quantitative comparison between morphological characteristics of entire colonies and genetic data.     

Morphological phylogeny of <Emphasis Type="Italic">Geusibia</Emphasis> Jordan, 1932 (Siphonaptera: Leptopsyllidae) and the host–parasite relationship with pikas

Thirteen species of fleas of the genus Geusibia Jordan, 1932 were included in a cladistic analysis based on morphological characters. The results support Geusibia as a monophyletic group within Ctenophyllus Wagner, 1927 (sensu lato) and there are five diagnostic characters that distinguish Geusibia from related genera of Ctenophyllus (s. l). There is no evidence to support a subgeneric classification. We propose that G. ochotona Zhan, Cai & Wu, 1997 and G. lacertosa(Smit, 1975) are junior synonyms of G. torosa Jordan, 1932. After a reconciliation analysis, only two co-speciation events were found in the host–parasite association between Geusibia and pikas (Ochotona:Ochotonidae: Lagomorpha). Therefore, there are no co-evolutionary relationships between them, although a high host preference of Geusibiaspp. is recorded. The distribution and host selection of Geusibia, relative to host associations, are also discussed. Although most specimens of Geusibia are found on pikas, the host is not the definitive factor in the distribution of the genus. Some environmental factors and some host behaviors also determine the presence of Geusibia. Therefore, Geusibia is defined as a host-habitat-dependent flea     

Morphology of the quadrate in the Eocene anseriform Presbyornis and extant galloanserine birds

Despite the notoriety, phylogenetic significance, and large number of available specimens of Presbyornis, its cranial anatomy has never been studied in detail, and its quadrate has been partly misinterpreted. We studied five quadrates of Presbyornis that reveal features hitherto unknown in the anseriforms but otherwise present in galliforms. As a result, we analyzed the variable quadrate characters among all extant galloanserine families and identified synapomorphies and other morphological variation among the major galloanserine clades. In terms of quadrate morphology, Presbyornis is more plesiomorphic than any extant anseriform (including the Anhimidae) and shares ancestral galloanserine characters with the Megapodiidae, the earliest branch of extant galliforms. The quadrate's morphology is inconsistent with the currently accepted anseriform phylogeny that nests Presbyornis within the crown‐group as a close relative of the Anatidae. The presbyornithid quadrates exhibit an unusual variation in the presence of a caudomedial pneumatic foramen, which we interpret as a result of a discontinuous change in the growth path of the pneumatic diverticulum. Another episode of morphogenetic imbalance in the growth path of the pneumatic diverticulum may have accompanied the disappearance of the basiorbital pneumatic foramen (along with the pneumatization of the pterygoid) at the origin of the crown‐group anseriforms. This episode is marked by the striking individual variation in the presence and location of pneumatic foramina in the mandibular part of the quadrate in the Anhimidae. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

Challenges in the delimitation of morphologically similar species: a case study of <Emphasis Type="Italic">Tuber brumale</Emphasis> agg. (Ascomycota,Pezizales)

Tuber brumale (winter truffle) is one of the most controversial true truffles, not only in regard to its ecological and economical role but also its taxonomy. Multilocus phylogenetic analyses have revealed that specimens identified earlier as T. brumale belong to two species. These species were deemed cryptic right away, because preliminary morphological measurements did not show any phenotypical differences. In this study, we measured the morphology of 119 T. brumale agg. specimens, identified by DNA-based phylogenetic tools. We found several continuous morphological characters which show strong statistical differences between the two species, albeit not without overlap. Using a combination of these characters, we show that efficient separation of the two species is possible. We describe T. cryptobrumale sp. nov. and present the environmental demands and the potential area reconstruction of both species. We argue that non-representative sampling is a major culprit in most failures to detect both the existence of morphologically similar species and their morphological differences. Our findings illustrate the benefits of integrative taxonomy: the use of a combination of molecular, morphological and ecological tools.     

Trichoderma mienum sp. nov., isolated from mushroom farms in Japan

During an investigation of Hypocrea/Trichoderma species inhabiting mushroom bedlogs, we found five strains of an undescribed species from a culture collection. These were analyzed using a combined approach, including morphology of holomorph, cultural studies, and phylogenetic analyses of the rRNA gene cluster of the internal transcribed spacer region, translation elongation factor 1-α, and RNA polymerase subunit II gene sequences. Distinctive morphological characters include stromata with green ascospores produced on potato dextrose agar medium, and Gliocladium-like to irregularly Verticillium-like conidiophores. In phylogenetic analyses, this species belongs to the Semiorbis clade, but its morphological characteristics do not match the other members of this clade. Based on morphological observations and phylogenetic analyses, we describe this as a new species, Trichoderma mienum, representing its Hypocrea teleomorph and Trichoderma anamorph.     

Morphology and phylogenetic significance of the pectoral articular region in elasmobranchs (Chondrichthyes)

The morphology of the articular region of the scapulocoracoid and the basal cartilages of the pectoral fin endoskeleton of elasmobranchs is reviewed in detail. Examination of this specific morphology in more than 140 species of elasmobranchs (of which 40 are reported here) revealed characters that may have a bearing on the higher‐level phylogeny of the group. Ten distinct characters of the scapular articular region of elasmobranchs are described, varying in terms of the number of distinct articular sites as well as their specific morphology (e.g. whether the articular surface is composed of condyles and/or facets). Previous interpretations of the articular region in morphological phylogenies are also reviewed, revealing much more morphological variation than formerly reported. These prior characters played an important role in supporting the Hypnosqualea, and may still be derived for this clade. The variation and distribution of the new characters discussed provide new insights for the evolution of the pectoral endoskeleton in chondrichthyans. They also highlight the continued importance of morphological characters for phylogenetic studies, and reinforce the necessity of in‐depth anatomical reviews of certain characters employed in previous higher‐level phylogenetic studies of elasmobranchs. © 2015 The Linnean Society of London     

The ochotonids of Eurasia: Biochronology and taxonomic diversity

The ochotonid faunas of Eurasia and North America from the Oligocene to the present time are reviewed. The pika family (Ochotonidae Thomas 1897) belongs to the order Lagomorpha, which includes five families: Ochotonidae, Mimotonidae Li 1978, Leporidae Fischer 1817 (hares), Palaeolagidae Dice 1929, and Prolagidae Gureev 1960. The family Ochotonidae consists of two subfamilies: Sinolagomyinae Gureev, 1960 and Ochotoninae Thomas, 1897 and comprises a total of 17 genera. Originating in Central Asia at the beginning of the Late Oligocene, pikas flourished during the Late Oligocene. The highest taxonomic diversity of pikas can be found in the Miocene and Pliocene; towards the Pleistocene, the ochotonid fauna declined. Only one genus, Ochotona, remained extant by the end of the Pleistocene. The genus includes a total of 38 known extinct taxa and 28 extant species.     

Pollen diversity and its implications to the systematics of Poecilanthe (Fabaceae,Papilionoideae, Brongniartieae)

The small South-American genus Poecilanthe has a striking morphological diversity in leaf type, inflorescence, seed morphology and chemical composition. Recent phylogenetic work also shows that Poecilanthe is paraphyletic. Despite the importance of palynology to better understand morphological diversity and potentially inform evolutionary analyses, the pollen morphology of Poecilanthe and most of its close relatives is unknown. This study uses light and electronic microscopy to describe the pollen morphology of eight species of Poecilanthe and the four related genera Ormosia, Harpalyce, Clathrotropis and Cyclolobium. We found pollen grains colpate only in four species of Poecilanthe and Harpalyce brasiliana and colporate pollen grains in the other four Poecilanthe species and the other related genera (Ormosia, Clathrotropis and Cyclolobium). An identification key for pollen of all species is provided. Using principal component analyses (PCA) we found that pollen grains of the Poecilanthe have considerable diversity. However, only limited correspondence between the PCA clusters and the Poecilanthe clades was found, suggesting that pollinic characters do not reflect evolutionary history in this group.     

Using Ultraconserved Elements to Unravel Lagomorph Phylogenetic Relationships

Journal of Mammalian Evolution - Lagomorpha (lagomorphs), the order of mammals including pikas, hares, and rabbits, is distributed on all continents. The order currently is hypothesized to comprise...     

Compilation of morphological and molecular data,a necessity for taxonomy: The case of Hormogaster abbatissae sp. n. (Annelida,Clitellata, Hormogastridae)

Conflict among data sources can be frequent in evolutionary biology, especially in cases where one character set poses limitations to resolution. Earthworm taxonomy, for example, remains a challenge because of the limited number of morphological characters taxonomically valuable. An explanation to this may be morphological convergence due to adaptation to a homogeneous habitat, resulting in high degrees of homoplasy. This sometimes impedes clear morphological diagnosis of species. Combination of morphology with molecular techniques has recently aided taxonomy in many groups difficult to delimit morphologically. Here we apply an integrative approach by combining morphological and molecular data, including also some ecological features, to describe a new earthworm species in the family Hormogastridae, Hormogaster abbatissae sp. n., collected in Sant Joan de les Abadesses (Girona, Spain). Its anatomical and morphological characters are discussed in relation to the most similar Hormogastridae species, which are not the closest species in a phylogenetic analysis of molecular data. Species delimitation using the GMYC method and genetic divergences with the closest species are also considered. The information supplied by the morphological and molecular sources is contradictory, and thus we discuss issues with species delimitation in other similar situations. Decisions should be based on a profound knowledge of the morphology of the studied group but results from molecular analyses should also be considered.     

An Intriguing Shift Occurs in the Novel Protein Phosphatase 1 Binding Partner,TCTEX1D4: Evidence of Positive Selection in a Pika Model

T-complex testis expressed protein 1 domain containing 4 (TCTEX1D4) contains the canonical phosphoprotein phosphatase 1 (PPP1) binding motif, composed by the amino acid sequence RVSF. We identified and validated the binding of TCTEX1D4 to PPP1 and demonstrated that indeed this protein is a novel PPP1 interacting protein. Analyses of twenty-one mammalian species available in public databases and seven Lagomorpha sequences obtained in this work showed that the PPP1 binding motif ₉₀RVSF₉₃ is present in all of them and is flanked by a palindromic sequence, PLGS, except in three species of pikas (Ochotona princeps, O. dauurica and O. pusilla). Furthermore, for the Ochotona species an extra glycosylation site, motif ₉₆NLS₉₈, and the loss of the palindromic sequence were observed. Comparison with other lagomorphs suggests that this event happened before the Ochotona radiation. The d_N/d_S for the sequence region comprising the PPP1 binding motif and the flanking palindrome highly supports the hypothesis that for Ochotona species this region has been evolving under positive selection. In addition, mutational screening shows that the ability of pikas TCTEX1D4 to bind to PPP1 is maintained, although the PPP1 binding motif is disrupted, and the N- and C-terminal surrounding residues are also abrogated. These observations suggest pika as an ideal model to study novel PPP1 complexes regulatory mechanisms.     

Diversity of diazotrophic gut inhabitants of pikas (Ochotonidae) revealed by PCR-DGGE analysis

Diazotrophic gut symbionts are considered to act as nitrogen providers for their hosts, as was shown for various termite species. Although the diet of lagomorphs, like pikas or rabbits, is very poor in nitrogen and energy, their fecal matter contains 30–40% of protein. Since our hypothesis was that pikas maintained a diazotrophic consortium in their gastrointestinal tract, we conducted the first investigation of microbial diversity in pika guts. We obtained gut samples from animals of several Ochotona species, O. hyperborea (Northern pika), O. mantchurica (Manchurian pika), and O. dauurica (Daurian pika), in order to retrieve and compare the nitrogen-fixing communities of different pika species. The age and gender of the animals were taken into consideration. We amplified 320-bp long fragments of the nifH gene using the DNA extracted directly from the colon and cecum samples of pika’s gut, resolved them by DGGE, and performed phylogenetic reconstruction of 51 sequences obtained from excised bands. No significant difference was detected between the nitrogen-fixing gut inhabitants of different pika species. NifH sequences fell into two clusters. The first cluster contained the sequences affiliated with NifH Cluster I (Zehr et al., 2003) with similarity to Sphingomonas sp., Bradyrhizobium sp., and various uncultured bacteria from soil and rhizosphere. Sequences from the second group were related to Treponema sp., Fibrobacter succinogenes, and uncultured clones from the guts of various termites and belonged to NifH Cluster III. We suggest that diazotrophic organisms from the second cluster are genuine endosymbionts of pikas and provide nitrogen for further synthesis processes thus allowing these animals not to be short of protein.     

Phylogeny and Reclassification of Hemistasia phaeocysticola (Scherffel) Elbrächter & Schnepf, 1996

Hemistasia phaeocysticola is a marine flagellate that preys on diatoms and dinoflagellates among others. Although its morphology and ultrastructure were previously observed and characterized, its phylogenetic position has not been analyzed using molecular sequence data. This flagellate was classified as a kinetoplastid on the basis of the presence of a kinetoplast in the mitochondrion. However, several morphological characteristics similar to those of diplonemids, a sister group of kinetoplastids, have also been noted. Herein, we report that H. phaeocysticola branches within the diplonemid clade in the phylogenetic tree reconstructed by analyzing 18S rRNA gene sequences. Its systematic placement based on this finding is also discussed.