Molecular Systematics Group

Evolutionary molecular systematics
of vertebrates

Research

According to mitogenomic studies, the bichir, Polypterus sp, (above) and the African lungfish, Protopterus annectens, (below) have basal positions in the evolutionary tree of gnathostomous fishes.  Images courtesy of and copyright Fredrik Sundström (above) and Oregon Zoo (below).

The use of molecular data has revolutionized the field of phylogenetics. The advantages of using DNA sequence data include: (i) the large number of analyzable characters; (ii) the discrete nature of these characters and the ability to mathematically model their pattern of evolution; (iii) the use of unequivocal rooting to establish the direction of evolution in a given tree and (iv) the ability to estimate evolutionary divergence times, providing a solidly supported fossil dating can be assigned to at least one node in the tree.

The particular aim of our project has been to construct phylogenies which show the direction of evolution in the vertebrate tree. To date our research has to a great extent been based on mitochondrial (mt) DNA molecules that have been sequenced in their entirety. Since the mt genomes have finite length the upcoming research will to a greater extent be based on nuclear data sets. The following account gives some details of our phylogenetic results based on mtDNA. The number of complete mtDNAs sequenced by members of our group is in the excess of 100 (not all published and analysed). Initially our studies were aimed at eutherian relationships but currently they include all classes of gnathostomous (jawed) vertebrates: Pisces, Amphibia, Reptilia, Aves and Mammalia.

This figure provides an outline of vertebrate phylogeny as evidenced in phylogenetic analyses of mt genomes. Numerals to the right give the number of mitochondrial genomes sequenced. The figure will open in a separate window which you can keep in the background for easy reference while reading.
 

A. Basal gnathostome relationships

Knowledge of the relationship between fishes and terrestrial vertebrates (tetrapods) is fundamental to understanding vertebrate evolution as a whole, and thus to virtually all comparative studies of the vertebrates. Morphological and molecular investigations into this relationship have focused primarily on whether the lungfishes or the coelacanths are the sister group of the tetrapods. In 1981, Rosen et al. formalized the hypothesis that the lungfishes are the closest relatives of the terrestrial vertebrates. The study of Rosen et al. revived the ”Huxleyian phylogeny”, introduced in the late 19th century. According to Rosen et al.s’ phylogeny, the coelacanth, lungfishes and tetrapods form a monophyletic group, Sarcopterygii, to the exclusion of other bony fishes, Actinopterygii (ray-finned fishes: bichirs, chondrosteans, gars, bowfin and teleosts). In this phylogeny tetrapods merely constitute a group of lobe-finned fishes.

In contrast to Rosen et al.s’ tree the first study of basal vertebrate relationships using both complete mtDNAs and unequivocal, non-gnathostomous rooting (lamprey, hagfish, echinoderms), showed that the bony fishes formed one group while the amniotes formed a separate group (Rasmussen et al. 1998). If these findings were phylogenetically correct, no extant gnathostomous fish could be designated as the sister group of the amniotes. The tree had the lungfish (Dipnoi) and the bichir (Cladistia) in a basal position on the piscine branch. These lung-possessing taxa were followed by the coelacanth and the teleosts. Thus, neither the monophyly of the Sarcopterygii, nor of the Actinopterygii were supported and neither the lungfishes nor the coelacanth were found to be the sister group of the tetrapods.

The famous coelacanth, Latimeria chalumnae, in its natural environment. Mitogenomic studies do not place it as a sister group to the tetrapods.  Image courtesy of and copyright Hans Fricke.

Rasmussen et al.s’ (1998) results prompted the sequencing of complete mtDNAs from cartilaginous fishes. The first sequenced taxa were the spiny dogfish, Squalus acanthias, (Rasmussen and Arnason 1999a) and the starry skate, Raja radiata (Rasmussen and Arnason 1999b). These species were followed by the ratfish, Chimaera monstrosa, and the horn shark, Heterodontus forsteri, (Arnason et al. 2001). Inconsistent with previous understanding, analyses of these sequences placed the cartilaginous fishes among the bony fishes and not in a basal position as the sister group of all other gnathostomes.

The findings of Rasmussen et al. (1998), Rasmussen and Arnason (1999a,b) and Arnason et al. (2001) have raised several important phylogenetic questions about deep gnathostome divergences and gnathostome evolution. The results, if phylogenetically correct, suggest inter alia that the cartilaginous skeleton occurring in chondrichthyans, chondrostei (sturgeons) and some teleosts (e.g. fugu) is a derived characteristic relative to the piscine bony skeleton. The results also support the notion that lungs are a ”primitive” gnathostome characteristic relative to the piscine swim bladder and the absence of this organ in many fishes.

According to mitogenomic studies, the nurse shark and the sting ray, both chondrichthyans, are not basal to other gnathostomes and their cartilaginous skeleton is a derived character.  Images courtesy of Dong Lin (shark) and Glenn and Martha Vargas (ray), both © California Academy of Sciences.

Since the publication of Rosen et al.s’ paper the hypothesis of a sister group relationship between lungfishes and tetrapods has become a doctrine in vertebrate evolution, with any inconsistent findings being regarded as incongruities, either in the data sets or in the analyses. Another commonly accepted theory is that the cartilaginous fishes (Chondrichthyes) are the sister group of all bony vertebrates, both bony fishes and tetrapods. Thus, the generally accepted gnathostome relationships can be summarized as: (outgroup, (cartilaginous fishes, (ray-finned fishes, (coelacanths, (lungfishes, tetrapods))))). From a palaeontological view the position of Chondrichthyes as the sister group of remaining gnathostomes is problematic as the oldest chondrichthyan fossils are considerably younger than those of for example the lungfishes.
 

B. Amphibia

Knowledge of the he evolutionary relationships between fishes, amphibians and amniotes (reptiles, birds and mammals) is important in understanding the transition of the vertebrates from aquatic to terrestrial life. We have recently sequenced the mt genomes of Ambystoma and Bufo melanostictus and used them in plylogenetic analyses together with the mtDNAs of Xenopus laevis and a caecilian, Typhlonectes natans. This sampling covers all basal amphibian lineages. The analyses identified monophyletic Amphibia, thereby challenging the ”Stockholm School” understanding that Amphibia are diphyletic.
 

C. Reptilia

The first complete reptilian mtDNA described was that of the alligator, Alligator mississippiensis (Janke and Arnason, 1997). Phylogenetic analyses including this sequence allowed examination of the relationship between Reptilia, Aves and Mammalia. This analysis reconstructed a sister group relationship between crocodiles and birds to the exclusion of mammals, inconsistent with the so-called Haematotherma hypothesis. Our study also provided an estimate of the time of separation between birds and crocodiles of 255 MYBP, a dating consistent with crocodilian palaeontology.

Analyses of the recently completed mt sequence of the iguana, Iguana iguana, and the caiman, Caiman crocodylus, in conjunction with the published sequences of turtles and a snake have allowed examination of the relationships between between all four of the main groups of reptiles (Janke et al. 2001).
 

D. Aves

The traditional avian phylogenetic tree depicts a basal split between Palaeognathae and Neognathae. The general acceptance of this tree is to a large extent based on the comprehensive DNA/DNA hybridization studies performed by Sibley and Ahlquist (1990), which showed a basal split between Palaeognathae and Neognathae. However, mitogenomic analyses (e.g. Härlid et al. 1997, 1998; Härlid and Arnason 1999) do not unequivocally support Sibley and Ahlquist's (1990) conclusions. In particular these studies (see also Slack et al. 2003) have shown that the Passeriformes have a much more basal position in the avian tree than suggested in the analyses of Sibley and Ahlquist (1990).

Mitogenomic studies have shown that the passerines (represented here by one of Darwin's finches, middle) occupy a much more basal position among birds than traditionally assumed. Thus many molecular studies show essentially an unresolved relationship between palaeognaths (represented by an ostrich, left), passerines, and remaining birds (here represented by an albatross, right).  Images courtesy of: ostrich, © Corel Corporation; finch, © Joseph Dougherty and the Society for Environmental Education; albatross, Gerald and Buff Corsi © California Academy of Sciences.

E. Mammalia

Our mammalian studies encompass the three primary groups Monotremata, Marsupialia and Eutheria. The first marsupial mtDNA to be sequenced was that of the opossum, Didelphis virginiana, (Janke et al. 1994). When this mtDNA was studied together with the mt genome of the platypus, Ornithorhynchus anatinus, the analyses joined Monotremata and Marsupialia to the exclusion of Eutheria (Janke et al., 1996). This unexpected result supported the so-called Marsupionta hypothesis. Extended phylogenetic studies of this relationship based on nuclear data (Janke et al. 2002) and additional mt genomes (Nilsson et al. 2003, 2004 in press) have further corroborated the Marsupionta hypothesis. Nuclear data sets useful for studying this hypothesis are still somewhat limited. The marsupionta hypothesis will, therefore, become one of the main nuclear priorities of our group.

Marsupials have been a somewhat neglected group in regard to morphological and molecular phylogenetics. Infraclass Marsupialia consists of about 280 living species that are today only found in South America and Australia. South America, Antarctica and Australia were geologically (South-Gondwana) and zoogeographically connected until about 45 million years ago when Australia and Antarctica became separated. Antarctica and South America remained connected into Miocene times. In the early 1980s, Szalay (1982) suggested that the mouse-sized Chilean marsupial monito del monte, Dromiciops gliroides, was more closely related to the Australian marsupials (in particular kangaroos, koalas and possums) than to the South American marsupials. The relationship between Dromiciops and other marsupials has not be conclusively resolved, however, as different molecular studies have not yielded consistent results. The relationship between South American and Australian marsupials has been investigated in a recent study (Nilsson et al. 2004, in press), and a more extensive study of marsupial relationships has been planned. That study in conjunction with the molecular dating of various marsupial divergences should provide detailed information on the phylogenetic relationships of all seven marsupial orders. This mt study will in turn be followed-up in a study of nuclear data sets.

Mitogenomic analyses suggest that the Chilean marsupial monito del monte (Dromiciops gliroides), formerly included in the American opossum family, is a closer relative to some Australian marsupials. Dromiciops occupies forrests, especially those containing Chilean bamboo.  Image courtesy of and copyright Jaime E Jiménez.

All eutherian orders are by now represented by complete mt genomes. The unrooted molecular trees of eutherian relationships are essentially the same irrespective of whether the analyses have been based on mt data or nuclear data sets of reasonable size. However, the rooted trees differ in that the nuclear trees preferably place the root between the so-called African clade and remaining eutherians, while the mt analyses place the root between Erinaceomorpha (hedgehogs) and remaining eutherians, alternatively between Rodentia and other eutherian orders. An important issue in this discussion (e.g. Janke and Miazawa 2003) is the appropriateness of some protein-coding nuclear genes for phylogenetic analyses as their pattern of evolution may differ markedly from all acknowledged models for the evolution of such genes. Thus, the nuclear gene BRCA1, which is commonly used in phylogenetic analyses shows the same mutational rate for the three codon positions.

For details on the mt eutherian tree the reader should consult Arnason et al. (2002) and Arnason and Janke (2002). In the following we will exemplify our research in the discussion of two particular topics, the evolution of Cetartiodactyla and the molecular dating of primate divergences related to the evolution of Homo.
 

Cetartiodactyla

The Cetartiodactyla includes the two traditional orders Cetacea (whales, dolphins, porpoises) and Artiodactyla (even-toed ungulates such as cow, sheep, camels, pigs and hippopotamuses). Cetartiodactyla is a part of the superordinal group Cetferungulata, which also includes Pholidota (pangolins), Carnivora (e.g. cats, dogs) and Perissodactyla (e.g. horses, tapirs, rhinoceroses). The palaeontological record of the cetferungulates is superior to those of most other mammalian lineages. Because of this, we have been able to establish four molecular-palaeontological references that can be used for molecular estimates of the time of other mammalian divergences for which little or no palaeontological data is available. One of these references (A/C-60) is the divergence between ruminant artiodactyls (A) and cetaceans (C) 60 MYBP, million years before present, (Arnason and Gullberg 1996; Arnason et al. 1996a). Another reference related to cetacean evolution is O/M-35, i.e. the divergence between Odontoceti (toothed whales) and Mysticeti (baleen whales) set at the Eocene-Oligocene boundary, 35 MYBP (Arnason et al. 2000; Arnason et al. 2004a). The third reference is E/R-50, the divergence between Equidae (horses, E) and Rhinocerotidae (rhinoceroses, R) 50 MYBP (Arnason et al. 1996b, 1998) and the fourth reference is C/F-52, the divergence between Canoid (dog-like) and Feloid (cat-like) carnivorans set at 52 MYBP (Arnason et al. 2000). These references yield consistent datings when applied to different divergences in the mammalian phylogenetic tree. They also place the the divergence between Eutheria and Marsupialia at about the same time, approximately 135 MYBP.

In order to resolve deep artiodactyl divergences, we have sequenced and analysed the complete mtDNAs of the fin and the blue whales (which both belong to the baleen whales), the sperm whale (which belongs to the toothed whales), the pig (Ursing and Arnason 1998a), the hippopotamus (Ursing and Arnason 1998b) and the alpaca (Ursing et al. 2000). Classical approaches group hippopotamuses and pigs together, but our analyses reconstructed a sister group relationship between Hippopotamidae and Cetacea, making both Artiodactyla and Suidae (pigs plus hippopotamuses) paraphyletic. The sister group relationship between Hippopotamidae and Cetacea was identified by Irwin and Arnason (1994) and statistically conclusively supported by Ursing and Arnason (1998b). This relationship, which was subsequently confirmed in analyses of nuclear data, has also recently gained recognition in morphological and palaeontological studies.

The family Hippopotamidae is a sister group to the cetaceans, represented here by an orca. Traditionally the hippopotamus was grouped together with pigs in the family Suidae.  Images © Corel Corporation.

The complete mtDNA of the fin whale was described by Arnason et al. (1991a) and that of the blue whale by Arnason and Gullberg (1993). The sequencing of the two genomes was prompted by the findings (Spilliaert et al. 1991; Arnason et al. 1991b) that these two species can hybridize and produce female offspring that are not obligatorily sterile. Comparison between the two mtDNAs allowed an estimate of the degree of molecular difference that may exist between species which still can produce offspring (Xu et al. 1996b). According to our estimates (Arnason et al. 1996a) these two, the largest animal species that have ever existed, separated 6.5 MYBP ago or earlier.

The relationships among the Carnivora were examined in considerable detail in studies of two mtDNA genes, cytochrome b and 12S rDNA, from more than 30 species (Ledje and Arnason 1996a,b). Prior to this we had sequenced the mt genomes of the harbour (Arnason and Johnsson 1992) and grey (Arnason et al. 1993) seals. As a follow-up to these studies, we have sequenced the mtDNAs of the Northern sea lion, Eumetopias jubatus, and the walrus, Odobenus rosmarus, Arnason et al. (2002). These mt genomes, together with those of the domestic cat (Lopez et al. 1996), the dog (Kim et al. 1998) and the polar bear (Arnason et al. 2002), conclusively identified a sister group relationship between Odobenidae and Otariidae (sea lions, fur seals) to the exclusion of Phocidae (true seals). The results (Arnason et al. 2002, Arnason and Janke 2002) challenged recent morphological studies that have advocated a sister group relationship between Odobenidae and Phocidae to the exclusion of Otariidae.

The order Perissodactyla has three extant families: Equidae, Tapiridae and Rhinocerotidae. The palaeontological record of the perissodactyls is detailed and our analyses have aided in resolving deep perissodactyl relationships and in establishing the palaeontological-molecular E/R reference.
 

Dating primate divergences

Primate evolution, notably that of the great apes (Hominoidea, i.e. gibbons, siamangs, orangutans, gorillas, chimpanzees and Homo) has always attracted great attention among scientists as well as laymen. For a long time it was commonly believed that Homo was only distantly related to other great apes. However, in a highly influential paper published in 1967, Sarich and Wilson argued that hominoid divergences in general were much more recent than commonly believed at the time. Using as a molecular calibration point the divergence between Cercopithecoidea (e.g. baboon) and Hominoidea set at 30 MYBP, Sarich and Wilson thus argued that the divergence between Homo and Pan (chimpanzees) took place about 5 MYBP instead of the traditional 10-15 MYBP. Gradually, this proposal gained widespread acceptance and the 5 MYBP dating of the divergence between Pan and Homo became a common standard for calculating the time of other mammalian divergences. Sarich and Wilson’s (1967) estimate was based on the observation that the molecular distance between Homo, Pan and Gorilla was about 1/6th of that between any of these species and the baboon. Since Sarich and Wilson (1967) had placed the divergence between Cercopithecoidea and Hominoidea at 30 MYBP, the automatic outcome of Sarich and Wilson’s (1967) calculation was the the three species of great apes had separated about 5 MYBP (30/6 MYBP).

In order to examine Sarich and Wilson’s conclusions, we sequenced the mtDNAs of Homo and the common chimpanzee (Arnason et al. 1996b); the gorilla (Xu and Arnason 1996a); the Sumatran orangutan (Xu and Arnason 1996b); the white-handed gibbon (Arnason et al. 1996c), the baboon (Arnason et al. 1998) and the Barbary macaque (Arnason et al. 2000). We then used our molecular-palaeontological references A/C-60 (Arnason et al. 1996a), E/R-50 (Arnason et al. 1998) and O/M-35 (Arnason et al. 2000) to estimate the times of various primate divergences. These estimates suggested inter alia that the divergence between Cercopithecoidea and Hominoidea had taken place 45-50 MYBP and not at 30 MYBP as assumed by Sarich and Wilson (1967). As evident this shift in the age allocated to the Cercopithecoidea-Hominoidea calibration point will automatically affect the estimated time of the divergence between Pan and Homo by moving it further back.

Estimates based on different calibration points need to be mutually supportive. Similarly, these estimates must not be in conflict with the fossil record. Our estimate of the divergence between Pan and Homo about 10 MYBP is consistent with the palaeontological record of cetaceans, artiodactyls, carnivorans and perissodactyls, which is superior to that of other mammalian orders. In contrast, when we use as a calibration point the divergence between Cercopithecoidea and Hominoidea set at 30 MYBP (Sarich and Wilson’s 1967 study) the estimate places cetacean origin at about 30 MYBP, a date that is incompatible with the age of the oldest cetacean fossils, more than 50 MY. Similarly, Sarich and Wilson’s calibration point places the separation between Equidae and Rhinocerotidae at about 28 MYBP, a date that is incompatible with the age (about 48 MY) of the oldest fossils belonging to these lineages. If Sarich and Wilson’s (1967) estimates were correct they would also suggest that Eutheria originated about 80 MYBP. That date is inconsistent with the age of the oldest eutherian and marsupial fossils, more than 120 MY.

There has been a considerable progress in primate palaeontology since the publication of Sarich and Wilson’s (1967) paper. The oldest fossil, which unquestionably is on the Homo lineage is Orrorin tugenensis (Senut et al. 2001) and its age, more than 6 MY, palaeontologically refutes any estimates that have placed the divergence between Pan and Homo at any younger date. Orrorin had upright gait and considering its advanced morphological distinction it is likely that the divergence between Pan and Homo took place much earlier than the age of the Orrorin fossil itself.

Femurs of a chimpanzee (left) and Orrorin tugenensis (right), the latter showing traits associated with bipedal gait.  Image courtesy of and copyright Martin Pickford.

Based on analyses of mtDNA the oldest divergences of modern humans have been estimated to be about 1/30 of the divergence time between Pan and ancestral Homo (Vigilant et al. 1991). Using a date of 5 MYBP for the Pan-Homo split hence gives an estimate of about 170 000 YBP (Vigilant et al. 1991; Ingman et al. 2000) as the coalescence time of modern humans (mitochondrial Eve). Providing the method used to calculate the 170 000 YBP estimates (Vigilant et al 1991; Ingman et al. 2000) was correct, our proposed dating of about 10 MYBP for the Pan-Homo divergence gives an estimate of about 350 000 YBP for the origin of modern humans. That estimate would be consistent with the existence of human populations in Palestine some 200 000 YBP, whereas the traditional dating, 170 000 YBP or less, for the origin of modern humans is inconsistent with these archaeological finds.

The coalescence time for human Y-chromosome variation is similar to that of mtDNA, as shown by recent analyses of nine diallelic polymorphic sites on the human Y-chromosome (Hammer et al. 1998). It thus appears that most human mt and Y-chromosome variation was wiped out at about the same time. According to our estimates this occurred about 350 000 YBP (Arnason et al. 2000). We find it plausible that this bottleneck was not a geographical event but rather resulted from a reproductive isolation associated with the formation of the 2n=46 chromosome human karyotype. A model of this kind, with the initial bottleneck involving presumably just a few individuals (Arnason 1972, White 1978), would be consistent with the limited mt and Y-chromosome variation in recent humans compared to that of our closest relatives, the chimpanzees and the gorilla, which share great karyological similarities (banding patterns, number of chromosome satellites) with Homo, but have maintained a chromosome number of 2n=48. It would also explain the similar coalescence times of the human mt genome and Y-chromosome and provide a reason as to how free gene flow could have been obstructed between modern humans and their 2n=48 chromosome contemporaries without affecting the transfer of technological knowledge.
 

References

Anderson S, Bankier AT, Barrell BG, de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Ros BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290: 457-465.

Arnason U (1972) The role of chromosomal rearrangement in mammalian speciation with special reference to Cetacea and Pinnipedia. Hereditas 70: 113-118.

Arnason U, Gullberg A, Widegren B (1991a) The complete nucleotide sequence of the mitochondrial DNA of the fin whale. J Mol Evol 33: 556-568.

Arnason U, Spilliaert R, Palsdottir A, Arnason A (1991b) Molecular identification of hybrids between the two largest whale species, the blue whale (Balaenoptera musculus) and the fin whale (B. physalus). Hereditas 115: 183-189.

Arnason U, Johnsson E (1992) The complete mitochondrial DNA sequence of the harbor seal, Phoca vitulina. J Mol Evol 34: 493-505.

Arnason U, Gullberg A (1993) Comparison between the complete mtDNA sequences of the blue and the fin whale, two species that can hybridize in nature. J Mol Evol 37: 312-322.

Arnason U, Gullberg A, Johnsson E, Ledje C (1993) The nucleotide sequence of the mitochondrial DNA molecule of the grey seal, Halichoerus grypus, and a comparison with mitochondrial sequences of other true seals. J Mol Evol 37: 323-330.

Arnason U, Gullberg A (1996) Cytochrome b nucleotide sequences and the identification of five primary lineages of extant cetaceans. Mol Biol Evol 13: 407-417.

Arnason U, Gullberg A, Janke A, Xu X (1996a) Pattern and timing of evolutionary divergences among hominoids based on analyses of complete mtDNAs. J Mol Evol 43: 650-661.

Arnason U, Xu X, Gullberg A (1996b) Comparison between the complete mitochondrial DNA sequences of human and the common chimpanzee. J Mol Evol 42: 145-152.

Arnason U, Gullberg A, Xu X (1996c) A complete mitochondrial DNA molecule of the white-handed gibbon, Hylobates lar, and comparison among individual mitochondrial genes of all hominoid genera. Hereditas 124: 185-189.

Arnason U, Gullberg A, Janke A (1998) Molecular timing of primate divergences as estimated by two nonprimate calibration points. J Mol Evol 47: 718-727.

Arnason U, Gullberg A, Burguete AS, Janke A (2000a) Molecular estimates of primate divergences and new hypotheses for primate dispersal and the origin of modern humans. Hereditas 133: 217-28.

Arnason U, Gullberg A, Gretarsdottir S, Ursing B, Janke A (2000b) The mitochondrial genome of the sperm whale and a new molecular reference for estimating eutherian divergence dates. J Mol Evol 50: 569-578.

Arnason U, Gullberg A, Janke A (2001) Molecular phylogenetics of gnathostomous (jawed) fishes: old bones, new cartilage. Zool Scripta 30: 249-255.

Arnason U, Janke A (2002) Mitogenomic analyses of eutherian relationships. Cytogenetic and Genome Research 96: 20-32.

Arnason U, Adegoke JA, Bodin K, Born EW, Esa YB, Gullberg A, Nilsson M, Short RV, Xu X, Janke A (2002) Mammalian mitogenomic relationships and the root of the eutherian tree. Proc Natl Acad Sci USA 99: 8151-8156.

Arnason U, Gullberg A, Janke A (2004a) Mitogenomic analyses provide new insights into cetacean origin and evolution. Gene 333C: 27-34.

Arnason U, Gullberg A, Janke A, Joss J, Elmerot C (2004b) Mitogenomic analyses of deep gnathostome divergences: a fish is a fish. Gene 333C: 61-70.

Hammer MF, Karafet T, Rasanayagam A, Wood ET, Altheide TK, Jenkins T, Griffiths RC, Templeton AR, Zegura SL (1998) Out of Africa and back again: nested cladistic analysis of human Y chromosome variation. Mol Biol Evol 15: 427-441.

Härlid A, Janke A, Arnason U (1997) The mtDNA sequence of the ostrich and the divergence between paleognathous and neognathous birds. Mol Biol Evol 14: 754-761.

Härlid A, Janke A, Arnason U (1998) The complete mitochondrial genome of Rhea americana and early avian divergences. J Mol Evol 46: 669-679.

Härlid A, Arnason U (1999) Analyses of mitochondrial DNA nest ratite birds within the Neognathae: supporting a neotenous origin of ratite morphological characters. Proc R Soc London, B, 266: 305-309.

Ingman M, Kaessmann H, Paabo S, Gyllensten U (2000) Mitochondrial genome variation and the origin of modern humans. Nature 408: 708-713.

Irwin DM, Arnason U (1994) Cytochrome b gene of marine mammals: Phylogeny and evolution. J Mammalian Evol 2: 37-55.

Gemmell NJ, Janke A, Western PS, Watson JM, Paabo S, Graves JA (1994) Cloning and characterization of the platypus mitochondrial genome. J Mol Evol 39: 200-205.

Janke A, Gemmell NJ, Feldmaier-Fuchs G, von Haeseler A, Paabo S (1996) The mitochondrial genome of a monotreme - the platypus (Ornithorhynchus anatinus). J Mol Evol 42: 153-159.

Janke A, Arnason U (1997) The complete mitochondrial genome of Alligator mississippiensis and the separation between recent Archosauria (Birds and Crocodiles). Mol Biol Evol 14: 1266-1272.

Janke A, Erpenbeck D, Nilsson M, Arnason U (2001) The mitochondrial genomes of the iguana (Iguana iguana) and the caiman (Caiman crocodylus): implications for amniote phylogeny. Proc R Soc London, B, 268: 623-631.

Janke A, Magnell O, Wieczorek G, Westerman M, Arnason U (2002) Phylogenetic analysis of 18S rRNA and the mitochondrial genomes of the wombat, Vombatus ursinus, and the spiny anteater, Tachyglossus aculeatus: Increased support for the Marsupionta hypothesis. J Mol Evol 54: 71-80.

Kim KS, Lee SE, Jeong HW, Ha JH (1998) The complete nucleotide sequence of the domestic dog (Canis familiaris) mitochondrial genome. Mol Phylogenet Evol 10: 210-220.

Ledje C, Arnason U (1996a) Phylogenetic analyses of complete cytochrome b sequences of the order Carnivora with particular emphasis on the Caniformia. J Mol Evol 42: 135-144.

Ledje C, Arnason U (1996b) Phylogenetic relationships within caniform carnivores based on the analyses of the mitochondrial 12S rRNA gene. J Mol Evol 43: 641-649.

Lopez JV, Cevario S, O'Brien SJ (1996) Complete nucleotide sequences of the domestic cat (Felis catus) mitochondrial genome and a transposed mtDNA tandem repeat (Numt) in the nuclear genome. Genomics 33: 229-246.

Misawa K, Janke A (2003) Revisiting the Glires concept - phylogenetic analysis of nuclear sequences. Mol Phylogenet Evol 28:320-327.

Nilsson M, Gullberg A, Spotorno AE, Arnason U, Janke A (2003) Radiation of marsupials after the K/T-boundary: evidence from complete mitochondrial genomes. J Mol Evol 57: S3-S12 Suppl 1.

Nilsson MA, Arnason U, Spencer PB, Janke A (2004) Marsupial relationships and a timeline for marsupial radiation in South Gondwana. Gene 340: 189-196.

Rasmussen A-S, Janke A, Arnason U (1998) The mitochondrial DNA molecule of the hagfish (Myxine glutinosa) and consideration of vertebrate phylogenetic relationships. J Mol Evol 46: 382-388.

Rasmussen A-S, Arnason U (1999a) Phylogenetic studies of complete mitochondrial DNA molecules place cartilaginous fishes within the tree of bony fishes. J Mol Evol 48: 118-123.

Rasmussen A-S, Arnason U (1999b) Molecular studies suggest that cartilaginous fishes have a terminal position in the piscine tree. Proc Natl Acad Sci USA 96: 2177-2182.

Rosen DE, Forey PL, Gardiner BG, Patterson C (1981) Lungfishes, tetrapods, paleontology, and plesiomorphy. Bull Am Museum Natl History 167: 159-276.

Sarich VM, Wilson AC (1967) Immunological time scale for hominid evolution. Science 158:1200-1203.

Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y (2001) First hominid from the Miocene (Lukeino Formation, Kenya). C. R. Acad. Sci. Paris, Sciences de la Terre et des planètes 332: 137-144.

Sibley CG, Ahlquist JE (1990) Phylogeny and Classification of Birds: a Study in Molecular Evolution. Yale Univ. Press, New Haven.

Slack KE, Janke A, Penny D, Arnason U (2003) Two new avian mitochondrial genomes (penguin and goose) and a summary of bird and reptile mitogenomic features. Gene 302: 43-52.

Spilliaert R, Vikingsson G, Arnason U, Palsdottir A, Sigurjonsson J, Arnason A (1991) Species hybridization between a female blue whale (Balaenoptera musculus) and a male fin whale (B. physalus): Molecular and morphological documentation. J Heredity 82: 269-274.

Szalay FS (1982) A new appraisal of marsupial phylogeny and classification. In Carnivorous marsupials, vol. 2 (Archer M, ed). Sydney Australia, Royal Zoological Society of New South Wales, pp. 621-640.

Ursing BM, Arnason U (1998a) The complete mitochondrial DNA sequence of the pig (Sus scrofa). J Mol Evol 47: 302-306.

Ursing BM, Arnason U (1998b) Analyses of mitochondrial genomes strongly support a hippopotamus-whale clade. Proc R Soc London, B, 265: 2251-2255.

Ursing BM, Slack KE, Arnason U (2000) Subordinal artiodactyl relationships in the light of phylogenetic analysis of 12 mitochondrial protein-coding genes. Zool Scripta 29: 83-88.

Vigilant L, Stoneking M, Harpending H, Hawkes K, Wilson AC (1991) African populations and the evolution of human mitochondrial DNA. Science 253: 1503-1507.

White MJD (1978) Modes of Speciation, W. H. Freeman and Company, San Francisco, USA.

Xu X , Arnason U (1996a) A complete sequence of the mitochondrial genome of the western lowland gorilla. Mol Biol Evol 13: 691-698.

Xu X, Arnason U (1996b) The mitochondrial DNA molecule of Sumatran orangutan and a molecular proposal for two (Bornean and Sumatran) species of orangutan. J Mol Evol 43: 431-437.

Xu X, Janke A, Arnason U (1996a) The complete mitochondrial DNA sequence of the greater Indian rhinoceros, Rhinoceros unicornis, and the phylogenetic relationship among Carnivora, Perissodactyla and Artiodactyla (+ Cetacea). Mol Biol Evol 13: 1167-1173.

Xu X, Gullberg A, Arnason U (1996b) The complete mitochondrial DNA (mtDNA) of the donkey and mtDNA comparisons among four closely related mammalian species-pairs. J Mol Evol 43: 438-446.

Top of this page
Project home page
Department Home Page

Contact: Axel Janke, Associate Professor
Address:	Department of Cell and Organism Biology,  Genetics Building, Sölvegatan 29,  SE-223 62 Lund, Sweden
Phone: +46 46 222 78 49  Fax: +46 46 222 78 74 E-mail: Updated: 29 April 2008 Webmaster:

Dept Home    Research    Education