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Implications of biogeography of human populations for 'race' and medicine.

In this review, we focus on the biogeographical distribution of genetic variation and address whether or not populations cluster according to the popular concept of 'race'. We show that racial classifications are inadequate descriptors of the distribution of genetic variation in our species. Although populations do cluster by broad geographic regions, which generally correspond to socially recognized races, the distribution of genetic variation is quasicontinuous in clinal patterns related to geography. The broad global pattern reflects the accumulation of genetic drift associated with a recent African origin of modern humans, followed by expansion out of Africa and across the rest of the globe. Because disease genes may be geographically restricted due to mutation, genetic drift, migration and natural selection, knowledge of individual ancestry will be important for biomedical studies. Identifiers based on race will often be insufficient.

Biological Evolution↗

Mitochondrial DNA variation and biogeography of eastern gorillas.

Mitochondrial DNA variation in 109 individuals from four populations of wild living gorillas in East Africa was ascertained by sequencing the first hypervariable segment of the control region, or 'd-loop', amplified from noninvasively collected hair and faeces. D-loop haplotypes from eastern gorillas fell into two distinct clades, each with low levels of genetic diversity; most observed haplotypes within each clade differing by only one or two mutations. Both clades show evidence of population bottlenecks in the recent past, perhaps concomitant with the tropical forest reduction and fragmentation brought on by global cooling and drying associated with the last glacial maximum.

Africa↗

Historical biogeography and interspecific mtDNA introgression in Euhadra peliomphala (the Japanese land snail).

We assess variation in mitochondrial DNA (mtDNA) using partial sequences (560 bp) of the COI gene among populations of Japanese land snails, Euhadra peliomphala. Phylogeographical analysis reveals five primary clades that correspond basically to five discrete areas: the Boso Peninsula (B), the Kanto area (K), around Lake Ashinoko (A), the Northern Izu Peninsula (N), and the Southern Izu Peninsula (S). Although there are no current geographical barriers separating these five subpopulations, the borders between each area correspond to palaeogeographical events during the Pleistocene, such as volcanic activities and the disappearance of the landbridge between the Southern Boso area and the mainland of Japan. In addition, our analysis of isolation-by-distance and the distribution of pairwise sequence differences indicate that haplotypes of the B and K lineages have recently increased their population size exponentially. We have also discovered interspecific mtDNA introgression between E. peliomphala and the parapatric species E. brandtii at the contact zone in the Northern Kanto area. Unexpectedly, the E. brandtii-type mtDNA was also found in the populations of E. peliomphala in the Southern Boso area. Because recent contact between both species is unlikely, the introgressed mtDNA of E. brandtii could be a remnant of past hybridization, when E. peliomphala colonized this area via the landbridge that existed in the early Pleistocene.

Animals↗

Mitochondrial DNA diversity and historical biogeography of a wet forest-restricted frog (Litoria pearsoniana) from mid-east Australia.

MtDNA sequencing was used to investigate the genetic population structure of Litoria pearsoniana, a wet forest-restricted hylid frog, endemic to southeast Queensland and northeast New South Wales, Australia. L. pearsoniana is regarded as endangered under Queensland legislation. Significant genetic divergence among populations of frogs from different rainforest isolates was identified, but the lack of reciprocal monophyly among adjacent isolates suggests this is the result of a relatively recent disruption to gene flow. A paired catchment study within a single rainforest isolate, the Conondale Range, revealed no substantial genetic structuring, indicating the occurrence of terrestrial dispersal among nearby streams either in the recent past or currently. Two major reciprocally monophyletic clades of mtDNA alleles were identified. These corresponded to two geographical regions separated by the Brisbane River valley; one consisting of the Conondale and D'Aguilar Ranges, and the other of the southern isolates in the Main, Border and Gibraltar Ranges. Sequence divergence between the two regions was more consistent with a late Miocene or Pliocene rather than late Pleistocene separation, and is similar to that found among phylogeographic divisions of rainforest reptiles and amphibians in north Queensland rainforests. The molecular evidence for long-term separation of these two regions is corroborated by the pattern of species turnover in the distributions of species of rainforest-restricted amphibians and reptiles. Bioclimatic modelling suggests that appropriate conditions for L. pearsoniana would have been restricted to isolated refugees in each phylogeographic division under cooler and drier climates, such as predicted for the last glacial maximum. Currently isolated montane areas may have been connected transiently during the past 2000 years. Identification of long-term zoogeographic divisions among southeast Queensland rainforest herpetofauna has important implications for conservation and management. Conservation management of L. pearsoniana should be applied at the scale of major rainforest isolates and the conservation status of the species should be assessed independently north and south of the historical division.

Animals↗

Molecular systematics, biogeography and population structure of neotropical freshwater needlefishes of the genus Potamorrhaphis.

Phylogenetic relationships of populations and species within Potamorrhaphis, a genus of freshwater South American needlefishes, were assessed using mitochondrial cytochrome b sequences. Samples were obtained from eight widely distributed localities in the Amazon and Orinoco rivers, and represented all three currently recognized species of Potamorrhaphis. The phylogeny of haplotypes corresponded imperfectly to current morphological species identities: haplotypes from P. guianensis, the most widespread species, did not make up a monophyletic clade. Geography played a strong role in structuring genetic variation: no haplotypes were shared between any localities, indicating restricted gene flow. Possible causes of this pattern include limited dispersal and the effects of current and past geographical barriers. The haplotype phylogeny also showed a complex relationship between fishes from different river basins. Based on the geographical distribution of clades, we hypothesize a connection between the middle Orinoco and Amazon via rivers of the Guianas. More ancient divergence events may have resulted from Miocene alterations of river drainage patterns. We also present limited data for two other Neotropical freshwater needlefish genera: Belonion and Pseudotylosurus. Pseudotylosurus showed evidence of substantial gene flow between distant localities, indicating ecological differences from Potamorrhaphis.

Animals↗

Glacial vicariance and historical biogeography of rock ptarmigan (Lagopus mutus) in the Bering region.

In this paper, we address alternative hypotheses for the evolution of subspecies of rock ptarmigan (Lagopus mutus) endemic to the Aleutian Archipelago. To do this we examined patterns of genetic differentiation among populations of rock ptarmigan in the Aleutian Islands and parts of both Alaska and Siberia. Variation in mitochondrial control region sequences of 105 rock ptarmigan from 10 subspecies within the Bering region revealed three major phylogenetic lineages, two of which are endemic to the Aleutian Islands. Accordingly, haplotype and nucleotide diversities of rock ptarmigan within the archipelago are much higher than within mainland Alaska or Siberia. For Aleutian rock ptarmigan, analyses of molecular variance indicated significant genetic structuring and low estimates of gene flow among populations, despite small interisland distances within the archipelago. However, isolation by distance did not describe the pattern of gene flow or differentiation at this scale. Our estimates of divergence times of lineages suggest that Aleutian rock ptarmigan became isolated prior to the most recent Pleistocene glaciation event (late Wisconsin Stade) and that current patterns of genetic variation reflect the postglacial redistribution of divergent lineages and subsequent limited gene flow. In addition, genetic divergence among lineages was concordant with the distribution of plumage types among subspecies. The patterns of genetic variation described here for rock ptarmigan provide evidence for the role of glacial vicariance in contributing to genetic diversity within this and other Bering region species.

Alaska↗

Biogeography of a southern hemisphere freshwater fish: how important is marine dispersal?

Galaxias maculatus is one of the world's most widely distributed freshwater fish. This species has a marine-tolerant juvenile phase, and a geographical range extending through much of the southern hemisphere. We conducted phylogeographic analyses of 163 control region haplotypes of G. maculatus, including samples from New Zealand (five locations), Tasmania (one location) and Chile (one location). A lack of genetic structure among New Zealand samples suggests that marine dispersal facilitates considerable gene flow on an intra-continental scale. The discovery of a Tasmanian-like haplotype in one of 144 New Zealand samples indicates that inter-continental marine dispersal occurs but is insufficient to prevent mitochondrial DNA differentiation among continents. The sister relationship of Tasmanian and New Zealand clades implies that marine dispersal is an important biogeographical mechanism for this species. However, a vicariant role in the divergence of eastern and western Pacific G. maculatus cannot be rejected.

Animals↗

Historical biogeography in a linear system: genetic variation of sea rocket (Cakile maritima) and sea holly (Eryngium maritimum) along European coasts.

The exclusively coastal Cakile maritima and Eryngium maritimum represent a linear biogeographical system. Genetic variation among 25 individuals of C. maritima and 16 individuals of E. maritimum, from the coasts of Europe, North Africa and the Canary Islands, was analysed using random amplified polymorphic DNAs (RAPDs) and intersimple sequence repeats (ISSRs). Genetic distances (Dice) were calculated and used to investigate the correlation between genetic and geographical distances, to construct Neighbour Joining (NJ) trees, and to compare mean genetic distances between areas within and across species. Genetic distances and geographical distances measured along the coast are well correlated in Cakile and Eryngium. This implies that dispersal in both species is largely along the coast. The NJ analyses resulted in the recognition of Atlantic and Mediterranean clusters in both Cakile and Eryngium. The genetic distance between these two clusters is much larger in Eryngium (0. 285) than in Cakile (0.037). Mean genetic distances are substantially higher in the Mediterranean than in the Atlantic clusters in both species, and higher in Cakile than in Eryngium particularly in the Atlantic cluster. It is argued that all similarities and differences between the two species can be explained with the presumed distribution of the two species in the Würm glacial as reconstructed from their extant temperature requirements, the distribution of ice cover, permafrost, and sea surface temperatures in that period, and indirect fossil evidence.

Apiaceae↗

Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe.

Arabidopsis thaliana provides a useful model system for functional, evolutionary and ecological studies in plant biology. We have analysed natural genetic variation in A. thaliana in order to infer its biogeographical and historical distribution across Eurasia. We analysed 79 amplified fragment length polymorphism (AFLP) markers in 142 accessions from the species' native range, and found highly significant genetic isolation by distance among A. thaliana accessions from Eurasia and southern Europe. These spatial patterns of genetic variation suggest that A. thaliana colonized central and northern Europe from Asia and from Mediterranean Pleistocene refugia, a trend which has been identified in other species. Statistically significant levels of multilocus linkage disequilibrium suggest intermediate levels of disequilibrium among subsets of loci, and analysis of genetic relationships among accessions reveal a star or bush-like dendrogram with low bootstrap support. Taken together, it appears that there has been sufficient historical recombination in the A. thaliana genome such that accessions do not conform to a tree-like, bifurcating pattern of evolution - there is no 'ecotype phylogeny.' Nonetheless, significant isolation by distance provides a framework upon which studies of natural variation in A. thaliana may be designed and interpreted.

Arabidopsis↗

Population structure and biogeography of migratory freshwater fishes (Prochilodus: Characiformes) in major South American rivers.

Mitochondrial DNA (mtDNA) sequences were used to infer the phylogenetic relationships of Prochilodus species in the Paraná, Amazonas, Orinoco, and Magdalena basins. Sequences of ATPase subunits 6 and 8 (total 840 bp) were obtained for 21 Prochilodus specimens from the four river systems. Using Semaprochilodus as an outgroup, phylogenetic analyses showed that: (i) each river basin contains a monophyletic group of mtDNA lineages; and (ii) the branching order places Magdalena in a basal position with subsequent branching of Orinoco, Amazon and Paraná. The mitochondrial control region was sequenced for 26 P. lineatus (from the Paraná basin) and six other Prochilodus specimens from the Magdalena, Orinoco and Amazon. All 26 control region haplotypes were unique with sequence divergence ranging from 0.3 to 3.6%. The control region phylogeny is well resolved but phylogenetic structure is not associated with geography. For example, mtDNA haplotypes from the upper Paraná (Mogui Guassú) and the upper Bermejo, separated by at least 2600 km, have close genealogical ties. Phylogeographic analyses, including nested clade analysis, suggest high levels of gene flow within this basin.

Animals↗

Phylogeography of the yucca moth Tegeticula maculata: the role of historical biogeography in reconciling high genetic structure with limited speciation.

Tegeticula maculata is one of the most ancient and morphologically variable lineages within the yucca moths, yet has apparently undergone little diversification in comparison with much younger yucca moth lineages that have rapidly diversified. A phylogeographic approach was used to determine the number of independent lineages within T. maculata and to examine whether these patterns corresponded with morphological differences between its subspecies maculata and extranea. Phylogenetic analysis of mitochondrial DNA sequence variation indicated that the two subspecies are in separate clades, but there was also an equally deep split within subspecies maculata. There was no evidence for gene flow among regions and there was considerable substructure within clades. The phylogeographic structure of moth populations among and within subspecies can be explained in part by historical biogeographic boundaries and increasingly patchy postglacial distribution of the exclusive host plant, Hesperoyucca whipplei. Local specialization and co-adaptation would be possible in the absence of apparent gene flow, yet gross morphological divergence is limited to the very old split between the subspecies. Sorting of ancient mitochondrial lineages followed by local genetic differentiation may explain the pattern of high genetic structure with limited speciation.

Animals↗

Historical biogeography and molecular systematics of the Indo-Pacific genus Dascyllus (Teleostei: Pomacentridae).

The phylogeographical and systematic relationships among species in the tropical marine fish genus Dascyllus were inferred using mitochondrial DNA (mtDNA) sequence data. Although our results were generally consistent with previously published phylogenies based on both morphological and mitochondrial data, our broad taxonomic and geographical sampling design revealed novel insights into the phylogenetic history of Dascyllus that had escaped previous notice. These results include: (a) the polyphyletic nature of D. reticulatus mtDNAs, representing two divergent and geographically separated lineages, one shared with D. flavicaudus and the second forming the sister lineage of D. carneus; (b) the paraphyly of D. trimaculatus relative to the closely related D. abisella; and (c) phylogeographical structure within the widespread taxa D. aruanus and D. trimaculatus. Application of a molecular clock permits us to posit a causative role for tectonic and oceanic changes regarding some Dascyllus speciation events. Finally, we mapped body size and the presence or absence of protogynous sex change on the mtDNA tree, and tested published hypotheses regarding determinants of the evolution of mating system and protogyny in the genus. Our data rejected a model based on body size but not one based on phylogenetic inertia. The ability to change sex arose once in the ancestor to the entire genus, and was lost once in the ancestor of the D. trimaculatus complex. For taxa that are as geographically widespread as many Indo-Pacific genera, this study highlights the importance of adequate geographical sampling when inferring patterns of species diversification and life history evolution.

Animals↗

Holarctic phylogeography of the root vole (Microtus oeconomus): implications for late Quaternary biogeography of high latitudes.

A species-wide phylogeographical study of the root vole (Microtus oeconomus) was performed using the whole 1140 base pair mitochondrial (mt) cytochrome b gene. We examined 83 specimens from 52 localities resulting in 65 unique haplotypes. Our results demonstrate that the root vole is divided into four main mtDNA phylogenetic lineages that seem to have largely allopatric distributions. Net divergence estimates (2.0-3.5%) between phylogroups, as well as relatively high nucleotide diversity estimates within phylogroups, indicate that the distinct phylogeographical structure was initiated by historical events that predated the latest glaciation. European root voles are divided into a Northern and a Central mtDNA phylogroup. The mtDNA data in concert with fossil records imply that root voles remained north of the classical refugial areas in southern Europe during the last glacial period. The currently fragmented populations in central Europe belong to a single mtDNA phylogroup. The Central Asian and the North European lineages are separated by the Ural Mountains, a phylogeographical split also found in collared lemmings (Dicrostonyx) and the common vole (M. arvalis). The Beringian lineage occurs from eastern Russia through Alaska to northwestern Canada. This distribution is congruent with the traditional boundaries of the Beringian refugium and with phylogeographical work on other organisms. In conclusion, similarities between the phylogeographical patterns in the root vole and other rodents, such as Arctic and subarctic lemmings, as well as more temperate vole species, indicate that late Quaternary geological and climatic events played a strong role in structuring northern biotic communities.

Animals↗

Was there a second adaptive radiation of giant tortoises in the Indian Ocean? Using mitochondrial DNA to investigate speciation and biogeography of Aldabrachelys (Reptilia, Testudinidae).

A radiation of five species of giant tortoises (Cylindraspis) existed in the southwest Indian Ocean, on the Mascarene islands, and another (of Aldabrachelys) has been postulated on small islands north of Madagascar, from where at least eight nominal species have been named and up to five have been recently recognized. Of 37 specimens of Madagascan and small-island Aldabrachelys investigated by us, 23 yielded significant portions of a 428-base-pair (bp) fragment of mitochondrial (cytochrome b and tRNA-Glu), including type material of seven nominal species (A. arnoldi, A. dussumieri, A. hololissa, A. daudinii, A. sumierei, A. ponderosa and A. gouffei). These and nearly all the remaining specimens, including 15 additional captive individuals sequenced previously, show little variation. Thirty-three exhibit no differences and the remainder diverge by only 1-4 bp (0.23-0.93%). This contrasts with more widely accepted tortoise species which show much greater inter- and intraspecific differences. The non-Madagascan material examined may therefore only represent a single species and all specimens may come from Aldabra where the common haplotype is known to occur. The present study provides no evidence against the Madagascan origin for Aldabra tortoises suggested by a previous molecular phylogenetic analysis, the direction of marine currents and phylogeography of other reptiles in the area. Ancient mitochondrial DNA from the extinct subfossil A. grandidieri of Madagascar differs at 25 sites (5.8%) from all other Aldabrachelys samples examined here.

Adaptation, Biological↗

Historical biogeography of the catfish genus Hypostomus (Siluriformes: Loricariidae), with implications on the diversification of Neotropical ichthyofauna.

Tropical South America possesses the largest ichthyofauna of any continental region. To test whether palaeohydrological changes may have been the causes of such diversification, the 'hydrogeological' hypothesis, the phylogenetic relationships of 51 representatives of the catfish genus Hypostomus (Siluriformes: Loricariidae) were inferred using mitochondrial D-loop haplotype sequences. Specimens were collected in all main tropical South American rivers systems east to the Andes. The major interrelationships found with the D-loop data were confirmed with a subset of 21 species using complete internal transcribed spacer (ITS) region sequences. The phylogenetic analysis indicate that the genus Hypostomus can be divided into four monophyletic clades. The historical biogeographical analysis of each of these clades allows the identification of seven major cladogenetic events. Using calibrated D-loop and ITS molecular clocks, date estimations were attributed to each of these cladogenetic events allowing a linkage between four of them with documented hydrogeological changes. Comparisons with published distribution patterns of unrelated fish groups indicate that several of the reconstructed and dated hydrogeological-cladogenetic events may have acted at a large scale on the diversification of Neotropical freshwater fish fauna during late Tertiary.

Animals↗

Morphological homoplasy, life history evolution, and historical biogeography of plethodontid salamanders inferred from complete mitochondrial genomes.

The evolutionary history of the largest salamander family (Plethodontidae) is characterized by extreme morphological homoplasy. Analysis of the mechanisms generating such homoplasy requires an independent molecular phylogeny. To this end, we sequenced 24 complete mitochondrial genomes (22 plethodontids and two outgroup taxa), added data for three species from GenBank, and performed partitioned and unpartitioned Bayesian, maximum likelihood, and maximum parsimony phylogenetic analyses. We explored four dataset partitioning strategies to account for evolutionary process heterogeneity among genes and codon positions, all of which yielded increased model likelihoods and decreased numbers of supported nodes in the topologies (Bayesian posterior probability >0.95) relative to the unpartitioned analysis. Our phylogenetic analyses yielded congruent trees that contrast with the traditional morphology-based taxonomy; the monophyly of three of four major groups is rejected. Reanalysis of current hypotheses in light of these evolutionary relationships suggests that (i) a larval life history stage reevolved from a direct-developing ancestor multiple times; (ii) there is no phylogenetic support for the "Out of Appalachia" hypothesis of plethodontid origins; and (iii) novel scenarios must be reconstructed for the convergent evolution of projectile tongues, reduction in toe number, and specialization for defensive tail loss. Some of these scenarios imply morphological transformation series that proceed in the opposite direction than was previously thought. In addition, they suggest surprising evolutionary lability in traits previously interpreted to be conservative.

Animals↗

Anthropoid primates from the Oligocene of Pakistan (Bugti Hills): data on early anthropoid evolution and biogeography.

Asian tarsiid and sivaladapid primates maintained relictual distributions in southern Asia long after the extirpation of their close Holarctic relatives near the Eocene-Oligocene boundary. We report here the discovery of amphipithecid and eosimiid primates from Oligocene coastal deposits in Pakistan that demonstrate that stem anthropoids also survived in southern Asia beyond the climatic deterioration that characterized the Eocene-Oligocene transition. These fossils provide data on temporal and paleobiogeographic aspects of early anthropoid evolution and significantly expand the record of stem anthropoid evolution in the Paleogene of South Asia.

Animals↗

Riding the Ice Age El Nino? Pacific biogeography and evolution of Metrosideros subg. Metrosideros (Myrtaceae) inferred from nuclear ribosomal DNA.

Metrosideros subg. Metrosideros (Myrtaceae) comprises approximately 26 species distributed widely across the Pacific basin. They occur on the ancient Gondwanan landmasses of New Zealand and New Caledonia, as well as on the volcanic islands of the remote Pacific, from Melanesia to tropical Polynesia and the Bonin Island. Phylogenetic analysis based on nuclear ribosomal DNA spacer sequences from all named species showed Metrosideros umbellata of New Zealand as basal in the subgenus, with the remaining species falling into three monophyletic clades. One includes the seven New Caledonian species together with three daughters in western Oceania that probably dispersed during the mid/late Tertiary. A second contains six taxa located in east Melanesia and Samoa that may also have arisen from a mid/late Tertiary dispersal, in this instance from New Zealand. The third includes three New Zealand endemics along with all of the taxa in remote Polynesia and accounts for much of the total range of the subgenus. These dispersed taxa in Polynesia either are identical to the New Zealand species Metrosideros excelsa or differ by a single nucleotide change. We suggest that they are all derived from a Pleistocene dispersal out of New Zealand. A relatively recent dispersal is surprising, given that this wind-dispersed genus has occupied New Zealand for much of the Tertiary and that some of the islands in remote Polynesia date to at least the Miocene. We attribute this dramatic range expansion to climate change-specifically changes in wind flow patterns-in the southern hemisphere during worldwide glaciation.

Base Sequence↗