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The impact of Quaternary Ice Ages on mammalian evolution.

The Quaternary was a time of extensive evolution among mammals. Most living species arose at this time, and many of them show adaptations to peculiarly Quaternary environments. The latter include continental northern steppe and tundra, and the formation of lakes and offshore islands. Although some species evolved fixed adaptations to specialist habitats, others developed flexible adaptations enabling them to inhabit broad niches and to survive major environmental changes. Adaptation to short-term (migratory and seasonal) habitat change probably played a part in pre-adapting mammal species to the longer-term cyclical changes of the Quaternary. Fossil evidence indicates that environmental changes of the order of thousands of years have been sufficient to produce subspeciation, but speciation has typically required one hundred thousand to a few hundred thousand years, although there are both shorter and longer exceptions. The persistence of taxa in environments imposing strong selective regimes may have been important in forcing major adaptive change. Individual Milankovitch cycles are not necessarily implicated in this process, but nor did they generally inhibit evolutionary change among mammals: many evolutionary divergences built over multiple climatic cycles. Deduction of speciation timing requires input from fossils and modern phenotypic and breeding data, to complement and constrain mitochondrial DNA coalescence dates which appear commonly to overestimate taxic divergence dates and durations of speciation. Migrational and evolutionary responses to climate change are not mutually exclusive but, on the contrary, may be synergistic. Finally, preliminary analysis suggests that faunal turnover, including an important element of speciation, was elevated in the Quaternary compared with the Neogene, at least in some biomes. Macroevolutionary species selection or sorting has apparently resulted in a modern mammalian fauna enriched with fast-reproducing and/or adaptively generalist species.

Adaptation, Biological↗

Advanced formulation of base pair changes in the stem regions of ribosomal RNAs; its application to mitochondrial rRNAs for resolving the phylogeny of animals.

The ribosomal RNAs (rRNAs) of animal mitochondria, especially those of arthropod mitochondria, have a higher content of G:U and U:G base pairs in their stem regions than the nuclear rRNAs. Thus, the theoretical formulation of base pair changes is extended to incorporate the faster base pair changes A:U<-->G:U<-->G:C and U:A<-->U:G<-->C:G into the previous formulation of the slower base pair changes between A:U, G:C, C:G and U:A. The relative base pair change probability containing the faster and slower base pair changes is theoretically derived to estimate the divergence time of rRNAs under the influence of selection for these base pairs. Using the cartilaginous fish-teleost fish divergence and the crustacean-insect divergence as calibration points, the present method successfully predicts the divergence times of the main branches of animals: Deuterostomia and Protostomia diverged 9.2 x 10(8) years ago, the divergence of Echinodermata, Hemichordata and Cephalochordata succeedingly occurred during the period from 8 x 10(8) to 6 x 10(8) years ago, while Arthropoda, Annelida and Mollusca diverged almost concomitantly about 7 x 10(8) years ago. The dating for the divergence of Platyhelminthes and Cnidaria is traced back to 1.2 x 10(9) years ago. This result is consistent with the fossil records in the Stirling Range Formation of southwestern Australia, the Ediacara and Avalon faunas and the Cambrian Burgess Shale. Thus, the present method may be useful for estimating the divergence times of animals ranging from 10(8) to 10(9) years ago, resolving the difficult problems, e.g. deviation from rate constancy and large sampling variances, in the usual methods of treating apparent change rates between individual bases and/or base pairs.

Animals↗

Transition and transversion rate in the evolution of animal mitochondrial DNA.

We present a further application of the stochastic model previously described (Lanave et al., 1984, 1985) for measuring the nucleotide substitution rate in the mammalian evolution of the mitochondrial DNA (mtDNA). The applicability of this method depends on the validity of "stationarity conditions" (equal nucleotide frequencies at first, second and third silent codon positions in homologous protein coding genes). In the comparison of homologous sequences satisfying the stationarity condition at the silent sites, only the four codon families (quartets) for which both transitions and transversions are silent at the third position are considered here. This has allowed us to estimate the transition and transversion rates for any pair of species. We have analyzed the third silent codon position of the triplet rat-mouse-cow, of a series of slightly divergent primates and of two Drosophila species. In terms of two external dating input we have then determined the phylogenetic trees for rat, mouse, and cow as well as for a number of primates including man. The phylogenetic tree that we have derived for the triplet rat, mouse and cow agrees with that we had previously determined by analyzing the first, second and third silent codon positions (in both duets and quartets) of mt genes (Lanave et al., 1985). For primates our method leads to the following branching order from the oldest to the most recent: Gibbon, Orangutan, Gorilla, Chimpanzee and Man. In absolute time, fixing the distance Chimpanzee-Man as 5 million years (Myr) we estimate the dating of the divergence nodes as: Gorilla 7 Myr; Orangutan 16 Myr; Gibbon 20 Myr. In all cases analyzed, the transition rate has been found to be substantially higher than the transversion rate. Moreover we have found that the transition/transversion ratio is different in the various lineages. We suggest that this fact is probably related to the nucleotide frequencies at the third silent codon position.

Animals↗

Phylogeography of the New Zealand cicada Maoricicada campbelli based on mitochondrial DNA sequences: ancient clades associated with cenozoic environmental change.

New Zealand's isolation, its well-studied rapidly changing landscape, and its many examples of rampant speciation make it an excellent location for studying the process of genetic differentiation. Using 1520 base pairs of mitochondrial DNA from the cytochrome oxidase subunit I, ATPase subunits 6 and 8 and tRNA(Asp) genes, we detected two well-differentiated, parapatrically distributed clades within the widespread New Zealand cicada species Maoricicada campbelli that may prove to represent two species. The situation that we uncovered is unusual in that an ancient lineage with low genetic diversity is surrounded on three sides by two recently diverged lineages. Using a relaxed molecular clock model coupled with Bayesian statistics, we dated the earliest divergence within M. campbelli at 2.3 +/- 0.55 million years. Our data suggest that geological and climatological events of the late Pliocene divided a once-widespread species into northern and southern components and that near the middle of the Pleistocene the northern lineage began moving south eventually reaching the southern clade. The southern clade seems to have moved northward to only a limited extent. We discovered five potential zones of secondary contact through mountain passes that will be examined in future work. We predict that, as in North American periodical cicadas, contact between these highly differentiated lineages will exist but will not involve gene flow.

Adenosine Triphosphatases↗

Molecular timing of primate divergences as estimated by two nonprimate calibration points.

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 approximately 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.

Animals↗

Common precursor of lysozymes of hen egg-white and bacteriophage T4.

The lysozymes of hen egg-white and bacteriophage T4 have similar catalytic properties but their amino acid sequences are not homologous. The question therefore arises whether they are derived from a common ancestral protein or have arisen independently. On the basis of the data we have gathered, it is shown here that the two enzymes are similar in the conformation of their backbones, in their modes of binding substrates, in specific protein--substrate interactions and in their presumed modes of action. We conclude that the two enzymes have diverged from a common precursor. This seems to be the most convincing example to date of the divergence of proteins with nonhomologous amino acid sequences.

Animals↗

No evidence for menstrual synchrony in lesbian couples.

Menstrual synchrony was investigated in a sample of 29 cohabiting lesbian couples, ranging in age from 22 to 48 years. One or both partners kept prospective daily records of variables including menses onset dates, intimate contact, and sexual activity. All women reported daily intimate interaction with their partners; none reported intimate interaction with men. Despite these potentially optimal conditions for the manifestation of synchrony, the differences between dyad members in menses onset dates were distributed randomly, and there was no evidence of convergence. In fact, most dyads exhibited divergence of onset dates. Reasons for lack of synchrony in this sample are discussed; one conclusion is that there is no solid evidence that menstrual synchrony is a stable attribute of past or contemporary human populations.

Adult↗

Molecular systematics of hystricognath rodents: evidence from the mitochondrial 12S rRNA gene.

Nucleotide sequence variation among 22 representatives of 14 families of hystricognathid rodents was examined using an 814-bp region of the mitochondrial 12S ribosomal RNA (rRNA) gene composing domains I-III. The purpose of this study was twofold. First, the phylogenetic relationships among Old World phiomorph (primarily African) and New World caviomorph (primarily South American) families were investigated, with a special emphasis on testing hypotheses pertaining to the origin of New World families and the identification of major monophyletic groups. Second, divergence times derived from molecular data were compared to those suggested by the fossil record. The resultant 12S rRNA gene phylogeny, analyzed separately and in combination with other morphological and molecular data, supported a monophyletic Caviomorpha. This finding is counter to the idea of a multiple origin for the South American families. The most strongly supported relationships within the Caviomorpha were a monophyletic Octodontoidea (containing five families) and the placement of New World porcupines (family Erethizontidae) as the most divergent family. Although comparisons to other data were more equivocal, the most parsimonious 12S rRNA trees also supported a monophyletic Phiomorpha that could be subdivided into two major groups, a clade containing the Thryonomyoidea (Thryonomyidae and Petromuridae) plus Bathyergidae and the more divergent Hystricidae (Old World porcupines). No significant differences in rates of 12S rRNA gene divergence were observed for hystricognathids in comparison to other rodent groups. Although time since divergence estimates were influenced by the fossil dates chosen to calibrate absolute rates, the overall divergence times derived from both transversions only and Kimura corrected distances and calibrations using two independent dates revealed a divergence time between Old and New World groups dating in the Eocene.

Africa↗

Monophyly of the order Rodentia inferred from mitochondrial DNA sequences of the genes for 12S rRNA, 16S rRNA, and tRNA-valine.

A recent analysis of amino acid sequence data (Graur et al.) suggested that the mammalian order Rodentia is polyphyletic, in contrast to most morphological data, which support rodent monophyly. At issue is whether the hystricognath rodents, such as the guinea pig, represent an independent evolutionary lineage within mammals, separate from the sciurognath rodents. To resolve this problem, we sequenced a region (2,645 bp) of the mitochondrial genome of the guinea pig containing the complete 12S ribosomal RNA, 16S ribosomal RNA, and transfer RNA(VAL) genes for comparison with the available sciurognath and other mammalian sequences. Several methods of analysis and statistical tests of the data all show strong support for rodent monophyly (91%-98% bootstrap probability, or BP). Calibration with the mammalian fossil record suggests a Cretaceous date (107 mya) for the divergence of sciurognaths and hystricognaths. An older date (38 mya) for the controversial Mus-Rattus divergence also is supported by these data. Our neighbor-joining analyses of all available sequence data (25 genes) confirm that some individual genes support rodent polyphyly but that tandem analysis of all data does not. We propose that the conflicting results are due to several compounding factors. The unique biochemical properties of some hystricognath metabolic proteins, largely responsible for generating this controversy, may have a single explanation: a cascade effect resulting from inactivation of the zinc-binding abilities of insulin. After excluding six genes possibly affected by insulin inactivation, analyses of all available sequence data (7,117 nucleotide sites, 3,099 amino acid sites) resulted in strong support for rodent monophyly (94% BP for DNA sequences, 90% for protein sequences), which lends support to the insulin-cascade hypothesis.

Animals↗

Bayesian models of episodic evolution support a late precambrian explosive diversification of the Metazoa.

Multicellular animals, or Metazoa, appear in the fossil records between 575 and 509 million years ago (MYA). At odds with paleontological evidence, molecular estimates of basal metazoan divergences have been consistently older than 700 MYA. However, those date estimates were based on the molecular clock hypothesis, which is almost always violated. To relax this hypothesis, we have implemented a Bayesian approach to describe the change of evolutionary rate over time. Analysis of 22 genes from the nuclear and the mitochondrial genomes under the molecular clock assumption produced old date estimates, similar to those from previous studies. However, by allowing rates to vary in time and by taking small species-sampling fractions into account, we obtained much younger estimates, broadly consistent with the fossil records. In particular, the date of protostome-deuterostome divergence was on average 582 +/- 112 MYA. These results were found to be robust to specification of the model of rate change. The clock assumption thus had a dramatic effect on date estimation. However, our results appeared sensitive to the prior model of cladogenesis, although the oldest estimates (791 +/- 246 MYA) were obtained under a suboptimal model. Bayes posterior estimates of evolutionary rates indicated at least one major burst of molecular evolution at the end of the Precambrian when protostomes and deuterostomes diverged. We stress the importance of assumptions about rates on date estimation and suggest that the large discrepancies between the molecular and fossil dates of metazoan divergences might partly be due to biases in molecular date estimation.

Algorithms↗

Genomic data support the hominoid slowdown and an Early Oligocene estimate for the hominoid-cercopithecoid divergence.

Several lines of indirect evidence suggest that hominoids (apes and humans) and cercopithecoids (Old World monkeys) diverged around 23-25 Mya. Importantly, although this range of dates has been used as both an initial assumption and as a confirmation of results in many molecular-clock analyses, it has not been critically assessed on its own merits. In this article we test the robusticity of the 23- to 25-Mya estimate with approximately 150,000 base pairs of orthologous DNA sequence data from two cercopithecoids and two hominoids by using quartet analysis. This method is an improvement over other estimates of the hominoid-cercopithecoid divergence because it incorporates two calibration points, one each within cercopithecoids and hominoids, and tests for a statistically appropriate model of molecular evolution. Most comparisons reject rate constancy in favor of a model incorporating two rates of evolution, supporting the "hominoid slowdown" hypothesis. By using this model of molecular evolution, the hominoid-cercopithecoid divergence is estimated to range from 29.2 to 34.5 Mya, significantly older than most previous analyses. Hominoid-cercopithecoid divergence dates of 23-25 Mya fall outside of the confidence intervals estimated, suggesting that as much as one-third of ape evolution has not been paleontologically sampled. Identifying stem cercopithecoids or hominoids from this period will be difficult because derived features that define crown catarrhines need not be present in early members of these lineages. More sites that sample primate habitats from the Oligocene of Africa are needed to better understand early ape and Old World monkey evolution.

Animals↗

Testing the Cambrian explosion hypothesis by using a molecular dating technique.

Molecular studies have the potential to shed light on the origin of the animal phyla by providing independent estimates of the divergence times, but have been criticized for failing to account adequately for variation in rate of evolution. A method of dating divergence times from molecular data addresses the criticisms of earlier studies and provides more realistic, but wider, confidence intervals. The data are not compatible with the Cambrian explosion hypothesis as an explanation for the origin of metazoan phyla, and provide additional support for an extended period of Precambrian metazoan diversification.

Animals↗

Molecular studies suggest that cartilaginous fishes have a terminal position in the piscine tree.

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 approximately 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 approximately 420 million years before present.

Animals↗

Nucleotide sequence analysis of SA-OMVV, a visna-related ovine lentivirus: phylogenetic history of lentiviruses.

The nucleotide sequence analysis of the visna-related South African Ovine Maedi Visna virus (SA-OMVV) demonstrates extensive genetic polymorphism among ovine lentiviruses. Differences between visna virus and SA-OMVV proteins range from 8.5 to 35% mismatched amino acids. Moreover, there is a new open reading frame (orf W) in the central part of the genome. A phylogenetic history calibrated by the divergence and isolation dates of these two ovine lentiviruses shows that radiation of the lentiviridae family is a recent event. Visna virus and SA-OMVV evolved independent of each other for about 42 years. The inferred molecular clock was used to calculate the minimal time elapsed since the divergence of some lentiviruses: 93 years for ovine and caprine lentiviruses, 430 years for ungulate and primate lentiviruses, and roughly 200 years for HIV-1, HIV-2, and SIVAGM. BRU, ELI, and MAL HIV-1 isolates diverged in the early 1960s.

Amino Acid Sequence↗

Mitogenomic analyses place the gharial (Gavialis gangeticus) on the crocodile tree and provide pre-K/T divergence times for most crocodilians.

Based on morphological analyses, extant members of the order Crocodylia are divided into three families, Alligatoridae, Crocodylidae, and Gavialidae. Gavialidae includes one species, the gharial, Gavialis gangeticus. In this study we have examined crocodilian relationships in phylogenetic analyses of seven mitochondrial genomes that have been sequenced in their entirety. The analyses did not support the morphologically acknowledged separate position of the gharial in the crocodilian tree. Instead the gharial joined the false gharial (Tomistoma schlegelii) on a common branch that was shown to constitute a sister group to traditional Crocodylidae (less Tomistoma). Thus, the analyses suggest the recognition of only two Crocodylia families, Alligatoridae and Crocodylidae, with the latter encompassing traditional Crocodylidae plus Gavialis/Tomistoma. A molecular dating of the divergence between Alligatoridae and Crocodylidae suggests that this basal split among recent crocodilians took place approximately 140 million years before present, at the Jurassic/Cretaceous boundary. The results suggest that at least five crocodilian lineages survived the mass extinction at the KT boundary.

Alligators and Crocodiles↗

Molecular dating: ape bones agree with chicken entrails.

Molecular time estimates, especially those that employed the 310 million years ago (Mya) date of mammal-bird divergence as the calibration point, were criticized in recent publications. In this article, we estimate the divergence time of primates and rodents, primates and artiodactyls and the different great ape species by using two independent calibration-time ranges and maximally conservative error estimates. We observed a variation of approximately +/-15-20% for most of the molecular time estimates in the 10-100 Mya range. The estimated range of the primate-rodent divergence time, 84-121 Mya, includes the date obtained with the 310 million years calibration point (110 Mya). We conclude that molecular time estimates remain useful tools of evolutionary biology, although utmost caution is required when interpreting the results.

Animals↗

Novel alpha7-like nicotinic acetylcholine receptor subunits in the nematode Caenorhabditis elegans.

We have used reverse-transcription-polymerase chain reaction (RT-PCR) and DNA sequencing techniques to confirm the transcription of seven (six alpha and one non-alpha) novel candidate nicotinic acetylcholine receptor (nAChR) subunit-encoding genes identified in the genome sequence of the nematode Caenorhabditis elegans. Compared to vertebrate nAChR subunits, they most closely resemble the homomer-forming, neuronal alpha7 subunit. Comparison of the predicted amino acid sequences of the new nAChR subunits with those described previously in C. elegans reveals five subunits (four alpha and one non-alpha) which resemble the DEG-3-like group of subunits. To date, this highly divergent nAChR subunit group is unique to C. elegans. ACR-22 is the first non-alpha member of the DEG-3-like group of subunits to be identified. Two new members of the related ACR-16-like nAChR group of subunits have also been shown to be transcribed, making the ACR-16-like subunit group the largest in C. elegans. Residues in the alpha subunit second transmembrane region (M2) which contribute to the channel lining show variations with implications for channel function. For example, in ACR-22, the highly conserved 0' lysine of M2 is replaced by histidine. Restrained molecular dynamics simulations have been used to generate molecular models of homo-pentameric M2 helix bundles for the novel subunits, enabling identification and display of pore-lining and protein interface residues. The number and diversity of genes encoding C. elegans nAChR subunits with similarities to the homomer-forming vertebrate alpha7 subunits and the identification of related non-alpha subunits, only found in C. elegans to date, suggest that at least some of these subunits may contribute to heteromers in vivo.

Amino Acid Sequence↗

Pancreatic-type ribonuclease 1 gene duplications in rat species.

Mammalian pancreatic-type ribonucleases (RNases) 1 represent single-copy genes in the genome of most investigated mammalian species, including Mus musculus and other murid rodents. However, in six species belonging to the genus Rattus and closely related taxa, several paralogous gene products were identified by Southern blotting and PCR amplifications of genomic sequences. Phylogenies of nucleotide and derived amino acid sequences were reconstructed by several procedures, with three Mus species as outgroup. Duplications of the RNase 1 occurred after the divergence of Niviventer cremoriventer and Leopoldamys edwardsi from the other investigated species. Four groups of paralogous genes could be identified from specific amino acid sequence features in each of them. Low ratios of nonsynonymous-to-synonymous substitutions and the paucity of pseudogene features suggest functional gene products. One of the RNase 1 genes of R. norvegicus is expressed in the pancreas. RNases 1 were isolated from pancreatic tissues of R. rattus and R. exulans and submitted to N-terminal amino acid sequence analysis. In R. rattus, the orthologue of the expressed gene of R. norvegicus was identified, but in R. exulans, two paralogous gene products were found. The gene encoding for one of these had not yet been found by PCR amplification of genomic DNA. A well-defined group of orthologous sequences found in five investigated species codes for very basic RNases. Northern blot analysis showed expression of messenger RNA for this RNase in the spleen of R. norvegicus, but the protein product could not be identified. Evolutionary rates of RNase 1, expressed as nucleotide substitutions per site per 10(3) million years (Myr), vary between 5 and 9 in the lines leading to Mus, Niviventer, and Lepoldamys (on the basis of an ancestral date of mouse/rat divergence of 12.2 Myr) and between 20 and 50 in the lines to the other sequences after divergence from Niviventer and Leopoldamys (5.5 Myr).

Amino Acid Sequence↗