• A massively parallel sequencing approach uncovers ancient origins and high genetic variability of endangered Przewalski's horses

      Goto, Hiroki; Ryder, Oliver A.; Fisher, Allison R.; Schultz, Bryant; Kosakovsky Pond, Sergei L.; Nekrutenko, Anton; Makova, Kateryna D. (2011)
      The endangered Przewalski's horse is the closest relative of the domestic horse and is the only true wild horse species surviving today. The question of whether Przewalski's horse is the direct progenitor of domestic horse has been hotly debated. Studies of DNA diversity within Przewalski's horses have been sparse but are urgently needed to ensure their successful reintroduction to the wild. In an attempt to resolve the controversy surrounding the phylogenetic position and genetic diversity of Przewalski's horses, we used massively parallel sequencing technology to decipher the complete mitochondrial and partial nuclear genomes for all four surviving maternal lineages of Przewalski's horses. Unlike single-nucleotide polymorphism (SNP) typing usually affected by ascertainment bias, the present method is expected to be largely unbiased. Three mitochondrial haplotypes were discovered—two similar ones, haplotypes I/II, and one substantially divergent from the other two, haplotype III. Haplotypes I/II versus III did not cluster together on a phylogenetic tree, rejecting the monophyly of Przewalski's horse maternal lineages, and were estimated to split 0.117–0.186 Ma, significantly preceding horse domestication. In the phylogeny based on autosomal sequences, Przewalski's horses formed a monophyletic clade, separate from the Thoroughbred domestic horse lineage. Our results suggest that Przewalski's horses have ancient origins and are not the direct progenitors of domestic horses. The analysis of the vast amount of sequence data presented here suggests that Przewalski's and domestic horse lineages diverged at least 0.117 Ma but since then have retained ancestral genetic polymorphism and/or experienced gene flow.
    • An ancient icon reveals new mysteries: mummy DNA resurrects a cryptic species within the Nile crocodile

      Hekkala, Evon; Shirley, Matthew H.; Amato, George; Austin, James D.; Charter, Suellen J.; Thorbjarnarson, John; Vliet, Kent A.; Houck, Marlys L.; Desalle, Rob; Blum, Michael J. (2011)
      ...Our analyses reveal a cryptic evolutionary lineage within the Nile crocodile that elucidates the biogeographic history of the genus and clarifies long‐standing arguments over the species’ taxonomic identity and conservation status. An examination of crocodile mummy haplotypes indicates that the cryptic lineage corresponds to an earlier description of C. suchus and suggests that both African Crocodylus lineages historically inhabited the Nile River....
    • Comparative and demographic analysis of orang-utan genomes

      Locke, Devin P.; Hillier, LaDeana W.; Warren, Wesley C.; Worley, Kim C.; Nazareth, Lynne V.; Muzny, Donna M.; Yang, Shiaw-Pyng; Wang, Zhengyuan; Chinwalla, Asif T.; Minx, Pat; et al. (2011)
      ‘Orang-utan’ is derived from a Malay term meaning ‘man of the forest’ and aptly describes the southeast Asian great apes native to Sumatra and Borneo. The orang-utan species, Pongo abelii (Sumatran) and Pongo pygmaeus (Bornean), are the most phylogenetically distant great apes from humans, thereby providing an informative perspective on hominid evolution. Here we present a Sumatran orang-utan draft genome assembly and short read sequence data from five Sumatran and five Bornean orang-utan genomes. Our analyses reveal that, compared to other primates, the orang-utan genome has many unique features. Structural evolution of the orang-utan genome has proceeded much more slowly than other great apes, evidenced by fewer rearrangements, less segmental duplication, a lower rate of gene family turnover and surprisingly quiescent Alu repeats, which have played a major role in restructuring other primate genomes. We also describe a primate polymorphic neocentromere, found in both Pongo species, emphasizing the gradual evolution of orang-utan genome structure. Orang-utans have extremely low energy usage for a eutherian mammal1, far lower than their hominid relatives. Adding their genome to the repertoire of sequenced primates illuminates new signals of positive selection in several pathways including glycolipid metabolism. From the population perspective, both Pongo species are deeply diverse; however, Sumatran individuals possess greater diversity than their Bornean counterparts, and more species-specific variation. Our estimate of Bornean/Sumatran speciation time, 400,000 years ago, is more recent than most previous studies and underscores the complexity of the orang-utan speciation process. Despite a smaller modern census population size, the Sumatran effective population size (Ne) expanded exponentially relative to the ancestral Ne after the split, while Bornean Ne declined over the same period. Overall, the resources and analyses presented here offer new opportunities in evolutionary genomics, insights into hominid biology, and an extensive database of variation for conservation efforts.
    • Comparative biology of mammalian telomeres: hypotheses on ancestral states and the roles of telomeres in longevity determination: The comparative biology of mammalian telomeres

      Gomes, Nuno M. V.; Ryder, Oliver A.; Houck, Marlys L.; Charter, Suellen J.; Walker, William; Forsyth, Nicholas R.; Austad, Steven N.; Venditti, Chris; Pagel, Mark; Shay, Jerry W.; et al. (2011)
      ...We examined telomeres/telomerase in cultured cells from >?60 mammalian species to place different uses of telomeres in a broad mammalian context. Phylogeny?based statistical analysis reconstructed ancestral states. Our analysis suggested that the ancestral mammalian phenotype included short telomeres (
    • Genetic connectivity across marginal habitats: the elephants of the Namib Desert

      Ishida Yasuko; Van Coeverden de Groot Peter J.; Leggett Keith E. A.; Putnam, Andrea S.; Fox Virginia E.; Lai Jesse; Boag Peter T.; Georgiadis Nicholas J.; Roca Alfred L. (2016)
      Locally isolated populations in marginal habitats may be genetically distinctive and of heightened conservation concern. Elephants inhabiting the Namib Desert have been reported to show distinctive behavioral and phenotypic adaptations in that severely arid environment. The genetic distinctiveness of Namibian desert elephants relative to other African savanna elephant (Loxodonta africana ) populations has not been established. To investigate the genetic structure of elephants in Namibia, we determined the mitochondrial (mt) DNA control region sequences and genotyped 17 microsatellite loci in desert elephants (n = 8) from the Hoanib River catchment and the Hoarusib River catchment. We compared these to the genotypes of elephants (n = 77) from other localities in Namibia. The mtDNA haplotype sequences and frequencies among desert elephants were similar to those of elephants in Etosha National Park, the Huab River catchment, the Ugab River catchment, and central Kunene, although the geographically distant Caprivi Strip had different mtDNA haplotypes. Likewise, analysis of the microsatellite genotypes of desert‐dwelling elephants revealed that they were not genetically distinctive from Etosha elephants, and there was no evidence for isolation by distance across the Etosha region. These results, and a review of the historical record, suggest that a high learning capacity and long‐distance migrations allowed Namibian elephants to regularly shift their ranges to survive in the face of high variability in climate and in hunting pressure.
    • Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification

      Meredith, R.W.; Janecka, J.E.; Gatesy, J.; Ryder, Oliver A.; Fisher, C.A.; Teeling, E.C.; Goodbla, A.; Eizirik, E.; Simao, T.L.L.; Stadler, T.; et al. (2011)
      ...We constructed a molecular supermatrix for mammalian families and analyzed these data with likelihood-based methods and relaxed molecular clocks. Phylogenetic analyses resulted in a robust phylogeny with better resolution than phylogenies from supertree methods....
    • Implications of different species concepts for conserving biodiversity

      Frankham, Richard; Ballou, Jonathan D.; Dudash, Michele R.; Eldridge, Mark D.B.; Fenster, Charles B.; Lacy, Robert C.; Mendelson, Joseph R.; Porton, Ingrid J.; Ralls, Katherine; Ryder, Oliver A. (2012)
      The ~26 definitions of species often yield different numbers of species and disparate groupings, with financial, legal, biological and conservation implications. Using conservation genetic considerations, we demonstrate that different species concepts have a critical bearing on our ability to conserve species.... Consequently, we conclude that the diagnostic phylogenetic species concept is unsuitable for use in conservation contexts, especially for classifying allopatric populations.
    • Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix

      Springer, Mark S.; Meredith, Robert W.; Gatesy, John; Emerling, Christopher A.; Park, Jong; Rabosky, Daniel L.; Stadler, Tanja; Steiner, Cynthia C.; Ryder, Oliver A.; Janečka, Jan E.; et al. (2012)
      Phylogenetic relationships, divergence times, and patterns of biogeographic descent among primate species are both complex and contentious. Here, we generate a robust molecular phylogeny for 70 primate genera and 367 primate species based on a concatenation of 69 nuclear gene segments and ten mitochondrial gene sequences, most of which were extracted from GenBank. Relaxed clock analyses of divergence times with 14 fossil-calibrated nodes suggest that living Primates last shared a common ancestor 71–63 Ma, and that divergences within both Strepsirrhini and Haplorhini are entirely post-Cretaceous. These results are consistent with the hypothesis that the Cretaceous-Paleogene mass extinction of non-avian dinosaurs played an important role in the diversification of placental mammals. Previous queries into primate historical biogeography have suggested Africa, Asia, Europe, or North America as the ancestral area of crown primates, but were based on methods that were coopted from phylogeny reconstruction. By contrast, we analyzed our molecular phylogeny with two methods that were developed explicitly for ancestral area reconstruction, and find support for the hypothesis that the most recent common ancestor of living Primates resided in Asia. Analyses of primate macroevolutionary dynamics provide support for a diversification rate increase in the late Miocene, possibly in response to elevated global mean temperatures, and are consistent with the fossil record. By contrast, diversification analyses failed to detect evidence for rate-shift changes near the Eocene-Oligocene boundary even though the fossil record provides clear evidence for a major turnover event (“Grande Coupure”) at this time. Our results highlight the power and limitations of inferring diversification dynamics from molecular phylogenies, as well as the sensitivity of diversification analyses to different species concepts.
    • Molecular phylogeny and evolution of the Perissodactyla

      Steiner, Cynthia C.; Ryder, Oliver A. (2011)
      The evolution of perissodactyls (rhinoceroses, tapirs, and horses) has been well studied primarily because of their extensive fossil record. Nevertheless, controversy persists regarding relationships of some of the extant taxa, reflecting inconsistencies between molecular and morphological studies. Here we examine the phylogenetic relationships of 16 living perissodactyl species by concatenating two mitochondrial and nine nuclear genes, and we estimate their divergence times using a relaxed Bayesian molecular clock approach....
    • Molecular systematics of eastern North American Phalangodidae (Arachnida: Opiliones: Laniatores), demonstrating convergent morphological evolution in caves

      Hedin, Marshal; Thomas, Steven M.; (2010)
      The phalangodid harvestmen (Opiliones: Laniatores) fauna of the southeastern United States has remained obscure since original descriptions of many genera and species over 60 years ago. The obscurity of this interesting group is pervasive, with uncertainty regarding basic systematic information such as generic limits, species limits, and geographic distributions....
    • On the phylogeny of Mustelidae subfamilies: analysis of seventeen nuclear non-coding loci and mitochondrial complete genomes

      Yu, Li; Peng, Dan; Liu, Jiang; Luan, Pengtao; Liang, Lu; Lee, Hang; Lee, Muyeong; Ryder, Oliver A.; Zhang, Yaping (2011)
      Background Mustelidae, as the largest and most-diverse family of order Carnivora, comprises eight subfamilies. Phylogenetic relationships among these Mustelidae subfamilies remain argumentative subjects in recent years. One of the main reasons is that the mustelids represent a typical example of rapid evolutionary radiation and recent speciation event. Prior investigation has been concentrated on the application of different mitochondrial (mt) sequence and nuclear protein-coding data, herein we employ 17 nuclear non-coding loci (>15 kb), in conjunction with mt complete genome data (>16 kb), to clarify these enigmatic problems. Results The combined nuclear intron and mt genome analyses both robustly support that Taxidiinae diverged first, followed by Melinae. Lutrinae and Mustelinae are grouped together in all analyses with strong supports. The position of Helictidinae, however, is enigmatic because the mt genome analysis places it to the clade uniting Lutrinae and Mustelinae, whereas the nuclear intron analysis favores a novel view supporting a closer relationship of Helictidinae to Martinae. This finding emphasizes a need to add more data and include more taxa to resolve this problem. In addition, the molecular dating provides insights into the time scale of the origin and diversification of the Mustelidae subfamilies. Finally, the phylogenetic performances and limits of nuclear introns and mt genes are discussed in the context of Mustelidae phylogeny. Conclusion Our study not only brings new perspectives on the previously obscured phylogenetic relationships among Mustelidae subfamilies, but also provides another example demonstrating the effectiveness of nuclear non-coding loci for reconstructing evolutionary histories in a group that has undergone rapid bursts of speciation.
    • Phylogenetic utility of nuclear introns in interfamilial relationships of Caniformia (Order Carnivora)

      Yu, L.; Luan, P.-T.; Jin, W.; Ryder, Oliver A.; Chemnick, Leona G.; Davis, Heidi A.; Zhang, Y.-P. (2011)
      The monophyletic group Caniformia (dog-like carnivores) in the order Carnivora comprises 9 families. Except for the general consensus for the earliest divergence of Canidae and the grouping of Procyonidae and Mustelidae, conflicting phylogenetic hypotheses exist for the other caniformian families. In the present study, a data set comprising > 22 kb of 22 nuclear intron loci from 16 caniformian species is used to investigate the phylogenetic utility of nuclear introns in resolving the interfamilial relationships of Caniformia. Our phylogenetic analyses support Ailuridae as the sister taxon to a clade containing Procyonidae and Mustelidae, with Mephitinae being the sister taxon to all of them. The unresolved placements of Ursidae and Pinnipeds here emphasize a need to add more data and include more taxa to resolve this problem. The present study not only resolves some of the ambiguous relationships in Caniformia phylogeny but also shows that the noncoding nuclear markers can offer powerful complementary data for estimating the species tree. None of the newly developed introns here have previously been used for phylogeny reconstruction, thus increasing the spectrum of molecular markers available to mammalian systematics. Interestingly, all the newly developed intron data partitions exhibit intraindividual allele heterozygotes (IIAHs). There are 115 cases of IIAHs in total. The incorporation of IIAHs into phylogenetic analysis not only provides insights into the interfamilial relationships of Caniformia but also identifies two potential hybridization events occurred within Ursidae and Otariidae, respectively. Finally, the powers and pitfalls of phylogenetics using nuclear introns as markers are discussed in the context of Caniformia phylogeny.
    • Response to comment on "Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification"

      Murphy, W.J.; Janecka, J.E.; Stadler, T.; Eizirik, E.; Ryder, Oliver A. (2012)
      Bininda-Emonds and Purvis reanalyzed our mammalian phylogenetic supermatrix and claim that our results are not significantly different from their delayed-rise hypothesis. We show that our divergence times are ~11 million years later for placental inter- and intraordinal divergences—consistent with a post–Cretaceous-Paleogene (KPg) radiation of most modern mammalian orders—and find no support for the early Eocene delayed-rise hypothesis.