Ulfur Arnason

The concept of recent hominoid divergences has been a mainstay in molecular primatology since the 1970's. However, the ages allocated to the calibration points used to establish these divergence times and the estimates resulting from their application, notably the commonly accepted divergence between Pan (chimpanzees) and Homo 5 million years before present (MYBP), are now palaeontologically refutable. Here we estimate the ages of various primate divergences using three references with a more detailed fossil record than any of the traditional primate calibration points. Our findings suggest that the latter yield datings that are too recent by a factor of about two. For example, our estimates place the divergence between Pan and Homo 10.5–13 MYBP. The revised estimates of primate divergence times suggest a new hypothesis for primate evolution and dispersal: that the divergence between strepsirhines (lorises, lemurs) and anthropoids was contemporary with the break-up of Southern continents about 90 MYBP, with strepsirhines becoming isolated on Madagascar and later dispersing to Africa (and Asia) and anthropoids evolving in South America and subsequently colonizing Africa (and Asia), or possibly North America. In addition we present a new hypothesis, which accommodates the strikingly similar coalescence times for human mitochondrial DNA and the Y-chromosome. This hypothesis posits a common mitochondrial and Y-chromosome bottleneck about 400,000 years ago, associated with the origination of the human 2n = 46 karyotype, obstructing genetic exchange with the 2n = 48 Homo contemporaries.

The strict orthology of mitochondrial (mt) coding sequences has promoted their use in phylogenetic analyses at different levels. Here we present the results of a mitogenomic study (i.e., analysis based on the set of protein-coding genes from complete mt genomes) of 60 mammalian species. This number includes 11 new mt genomes. The sampling comprises all but one of the traditional eutherian orders. The previously unrepresented order Dermoptera (flying lemurs) fell within Primates as the sister group of Anthropoidea, making Primates paraphyletic. This relationship was strongly supported. Lipotyphla (“insectivores”) split into three distinct lineages: Erinaceomorpha, Tenrecomorpha, and Soricomorpha. Erinaceomorpha was the basal eutherian lineage. Sirenia (dugong) and Macroscelidea (elephant shrew) fell within the African clade. Pholidota (pangolin) joined the Cetferungulata as the sister group of Carnivora. The analyses identified monophyletic Pinnipedia with Otariidae (sea lions, fur seals) and Odobenidae (walruses) as sister groups to the exclusion of Phocidae (true seals).

Cartilaginous fishes (chondrichthyans) have traditionally been taken as an early offshoot among jawed vertebrates. To examine some crucial chondrichthyan relationships, we have sequenced the mitochondrial genomes of the holocephalanChimaera monstrosa(ratfish) and the basal galeomorph speciesHeterodontus francisci(horn shark) and analysed them together with the corresponding data set of several other chondrichthyans, teleosts, the coelacanth, the African lungfish and the bichir. The rooting point of the tree was established using unequivocal outgroups, the sea lamprey , the sea lancelet or echinoderms. The phylogenetic analyses identified monophyletic Chondrichthyes in a terminal position in the piscine tree, lending no support to the traditionally accepted basal position of cartilaginous fishes among extant gnathostomes. The findings suggest that the cartilage characterizing extant chondrichthyans is a retention of an embryonic condition, thus representing a derived rather than a primitive phylogenetic and developmental stage. Similarly, the analyses suggest that the open gill slits of neoselachians (sharks and rays) constitute a derived state compared to the operculum (gill cover) characterizing bony fishes and holocephalans. The analyses did not support the so‐called Squalea/Galea hypothesis which posits that batomorphs (sharks, rays) have arisen from recent selachians (sharks). Inconsistent with the common understanding of piscine and gnathostome evolution, the two taxa having lungs, the African lungfish and the bichir, had a basal position in the piscine tree. The findings put into question the phylogenetic validity of the taxonomic nomenclature attributed to various vertebrate, notably piscine, clades.

The phylogenetic position of the lesser hedgehog tenrec, Echinops telfairi, was studied on the basis of analysis of the concatenated sequences of 12 mitochondrial protein‐coding genes. In addition to the tenrec, the analysis included two other representatives of the insectivore order Lipotyphla, the hedgehog and the mole. The eutherian tree was rooted with three non‐eutherian mammalian taxa. The analysis joined the tenrec, the African elephant (order Proboscidea) and the aardvark (order Tubulidentata) on a common branch. The three lipotyphlan taxa, the tenrec (Tenrecidae), the mole (Talpidae) and the hedgehog (Erinaceidae) were dispersed in the eutherian tree, demonstrating lipotyphlan polyphyly.

Extant cetaceans are systematically divided into two suborders: Mysticeti (baleen whales) and Odontoceti (toothed whales). In this study, we have sequenced the complete mitochondrial (mt) genome of an odontocete, the sperm whale (Physeter macrocephalus), and included it in phylogenetic analyses together with the previously sequenced complete mtDNAs of two mysticetes (the fin and blue whales) and a number of other mammals, including five artiodactyls (the hippopotamus, cow, sheep, alpaca, and pig). The most strongly supported cetartiodactyl relationship was: outgroup,((pig, alpaca),((cow, sheep),(hippopotamus,(sperm whale,(baleen whales))))). As in previous analyses of complete mtDNAs, the sister-group relationship between the hippopotamus and the whales received strong support, making both Artiodactyla and Suiformes (pigs, peccaries, and hippopotamuses) paraphyletic. In addition, the analyses identified a sister-group relationship between Suina (the pig) and Tylopoda (the alpaca), although this relationship was not strongly supported. The paleontological records of both mysticetes and odontocetes extend into the Oligocene, suggesting that the mysticete and odontocete lineages diverged 32–34 million years before present (MYBP). Use of this divergence date and the complete mtDNAs of the sperm whale and the two baleen whales allowed the establishment of a new molecular reference, O/M-33, for dating other eutherian divergences. There was a general consistency between O/M-33 and the two previously established eutherian references, A/C-60 and E/R-50. Cetacean (whale) origin, i.e., the divergence between the hippopotamus and the cetaceans, was dated to ≈55 MYBP, while basal artiodactyl divergences were dated to ≥65 MYBP. Molecular estimates of Tertiary eutherian divergences were consistent with the fossil record.

The complete mitochondrial (mt) genome of the mole Talpa europaea was sequenced and included in phylogenetic analyses together with another lipotyphlan (insectivore) species, the hedgehog Erinaceus europaeus, and 22 other eutherian species plus three outgroup taxa (two marsupials and a monotreme). The phylogenetic analyses reconstructed a sister group relationship between the mole and the fruit bat Artibeus jamaicensis (order Chiroptera). The Talpa/Artibeus clade constitutes a sister clade of the cetferungulates, a clade including Cetacea, Artiodactyla, Perissodactyla, and Carnivora. A monophyletic relationship between the hedgehog and the mole was significantly rejected by maximum parsimony and maximum likelihood. Consistent with current systematic schemes, analyses of complete cytochrome b genes including the shrew Sorex araneus (family Soricidae) revealed a close relationship between Talpidae and Soricidae. The analyses of complete mtDNAs, along with the findings of other insectivore studies, challenge the maintenance of the order Lipotyphla as a taxonomic unit and support the elevation of the Soricomorpha (with the families Talpidae and Soricidae and possibly also the Solenodontidae and Tenrecidae) to the level of an order, as previously proposed in some morphological studies.

The Chondrichthyes (cartilaginous fishes) are commonly accepted as being sister group to the other extant Gnathostomata (jawed vertebrates). To clarify gnathostome relationships and to aid in resolving and dating the major piscine divergences, we have sequenced the complete mtDNA of the starry skate and have included it in phylogenetic analysis along with three squalomorph chondrichthyans—the common dogfish, the spiny dogfish, and the star spotted dogfish—and a number of bony fishes and amniotes. The direction of evolution within the gnathostome tree was established by rooting it with the most closely related non-gnathostome outgroup, the sea lamprey, as well as with some more distantly related taxa. The analyses placed the chondrichthyans in a terminal position in the piscine tree. These findings, which also suggest that the origin of the amniote lineage is older than the age of the oldest extant bony fishes (the lungfishes), challenge the evolutionary direction of several morphological characters that have been used in reconstructing gnathostome relationships. Applying as a calibration point the age of the oldest lungfish fossils, 400 million years, the molecular estimate placed the squalomorph/batomorph divergence at ≈190 million years before present. This dating is consistent with the occurrence of the earliest batomorph (skates and rays) fossils in the paleontological record. The split between gnathostome fishes and the amniote lineage was dated at ≈420 million years before present.

An outstanding problem in mammal phylogeny is the relationship of the aardvark (Orycteropus afer), the only living species of the order Tubulidentata, to the extant eutherian lineages. In order to examine this problem the complete mitochondrial DNA (mtDNA) molecule of the aardvark was sequenced and analysed. The aardvark tRNA-Ser (UCN) differs from that of other mammalian mtDNAs reported and appears to have reversed to the ancestral secondary structure of non-mammalian vertebrates and mitochondrial tRNAs in general. Phylogenetic analysis of 12 concatenated protein-coding genes (3325 amino acids) included the aardvark and 15 additional eutherians, two marsupials and a monotreme. The most strongly supported tree identified the aardvark as a sister group of a clade including the armadillo (Xenarthra) and the Cetferungulata (carnivores, perissodactyls, artiodactyls and cetaceans). By applying three molecular calibration points the divergence between the aardvark and armadillo-cetferungulates was estimated at ca. 90 million years before present.

The complete mitochondrial DNA (mtDNA) molecule of the hamadryas baboon, Papio hamadryas, was sequenced and included in a molecular analysis of 24 complete mammalian mtDNAs. The particular aim of the study was to time the divergence between Cercopithecoidea and Hominoidea. That divergence, set at 30 million years before present (MYBP) was a fundamental reference for the original proposal of recent hominoid divergences, according to which the split among gorilla, chimpanzee, and Homo took place 5 MYBP. In the present study the validity of the postulated 30 MYBP dating of the Cercopithecoidea/Hominoidea divergence was examined by applying two independent nonprimate molecular references, the divergence between artiodactyls and cetaceans set at 60 MYBP and that between Equidae and Rhinocerotidae set at 50 MYBP. After calibration for differences in evolutionary rates, application of the two references suggested that the Cercopithecoidea/Hominoidea divergence took place >50 MYBP. Consistent with the marked shift in the dating of the Cercopithecoidea/Hominoidea split, all hominoid divergences receive a much earlier dating. Thus the estimated date of the divergence between Pan (chimpanzee) and Homo is 10–13 MYBP and that between Gorilla and the Pan/Homo linage ≈17 MYBP. The same datings were obtained in an analysis of clocklike evolving genes. The findings show that recalculation is necessary of all molecular datings based directly or indirectly on a Cercopithecoidea/Hominoidea split 30 MYBP.