Paternal leakage of mitochondrial DNA in the great tit (Parus major)

Animal mitochondrial DNA is normally inherited clonally from a mother to all her offspring. Mitochondrial heteroplasmy, the occurrence of more than one mitochondrial haplotype within an individual, can be generated by relatively common somatic mutations within an individual, by heteroplasmy of the oocytes, or by paternal leakage of mitochondria during fertilization of an egg. This biparental inheritance has so far been reported only in mice, mussels, Drosophila, and humans. Here we present evidence that paternal leakage occurs in a bird, the great tit Parus major. The major and minor subspecies groups of the great tit mix in the middle Amur Valley in far-eastern Siberia, where we found a bird that possessed the very distinct haplotypes of the two groups. To our knowledge this is the first report of paternal leakage in birds.     

Ring species – Do they exist in birds?

According to current theory, the splitting of a single species into two is best observed by a ring of intergrading populations which occupy a ring-shaped distribution area and whose terminal populations not only meet but overlap and co-occur without or with only little hybridization. The three most discussed examples in birds are revisited here. The great tit complex (Parus major s. l.) turned out to be an assemblage of four subspecies groups forming a secondary ring of population. The herring gull/lesser black-backed gull complex (Larus argentatus s. l.) forms a circumpolar circle of intergrading populations, but lacks the crucial cornerstone, the geographical overlap. The greenish warbler complex (Phylloscopus trochiloides s. l.) is close to the ideal ring species, but the ring is not complete and the Siberian zone of overlap needs further clarification and characterisation.     

The strange blood: natural hybridization in primates

Hybridization between two closely related species is a natural evolutionary process that results in an admixture of previously isolated gene pools. The exchange of genes between species may accelerate adaptation and lead to the formation of new lineages. Hybridization can be regarded as one important evolutionary mechanism driving speciation processes. Although recent studies have highlighted the taxonomic breadth of natural hybridization in the primate order, information about primate hybridization is still limited compared to that about the hybridization of fish, birds, or other mammals. In primates, hybridization has occurred mainly between subspecies and species, but has also been detected between genera and even in the human lineage. Here we provide an overview of cases of natural hybridization in all major primate radiations. Our review emphasizes a phylogenetic approach. We use the data presented to discuss the impact of hybridization on taxonomy and conservation.     

Close relatedness between mitochondrial DNA from seven Anser goose species

The phylogenetic relationships of seven goose species and two of the subspecies representing the genus Anser were studied by approximately 1180 bp of mitochondrial DNA tRNAglu, control region and tRNAphe sequences. Despite obvious morphological and behavioural affinities among the species, their evolutionary relationships have not been studied previously. The small amount of genetic differentiation observed in the mitochondrial DNA indicates an extremely close evolutionary relationship between the Anser species. The sequence divergences between the species (0.9–5.5%) are among the lowest reported for avian species with speciation events of Anser geese dating to late Pliocene and Pleistocene. The species grouped into four mtDNA lineages: (1) snow and Ross’ goose, (2) greylag goose, (3) white‐fronted goose, and (4) bean, pink‐footed and lesser white‐fronted goose. The phylogenetic relationships of the most closely related species, bean, pink‐footed and lesser white‐fronted goose, indicate a period of rapid cladogenesis. The poor agreement between morphological relationships and the phylogenetic relationships indicated by mtDNA sequences implies that either ancestral polymorphism and lineage sorting, hybridization and introgression or convergent evolution has been involved.     

Colonisation and diversification of the blue tits (Parus caeruleus teneriffae-group) in the Canary Islands

The blue tit (Parus caeruleus teneriffae group) is proposed to have colonised the Canary Islands from North Africa according to an east-to-west stepping stone model, and today, the species group is divided into four subspecies, differing in morphological, acoustic, and ecological characters. This colonisation hypothesis was tested and the population structure between and within the islands studied using mitochondrial DNA sequences of the non-coding and relatively fast evolving control region. Our results suggest that one of the central islands, Tenerife, was colonised first and the other islands from there. Three of the presently recognised four subspecies are monophyletic, exception being the subspecies teneriffae, which consists of two monophyletic groups, the one including birds of Tenerife and La Gomera and the other birds of Gran Canaria. The Gran Canarian birds are well differentiated from birds of the other islands and should be given a subspecies status. In addition, the teneriffae subspecies group is clearly distinct from the European caeruleus group, and therefore the blue tit assemblage should be divided into two species.     

Population differentiation in the marginal populations of the great tit (Paridae: Parus major)

The major subspecies group of the great tit, Parus major , has experienced demographic and spatial expansions during the last century in several sites at the edges of its distribution range. These expansions, although temporarily very even, have resulted in dissimilar patterns of molecular diversity. Populations locating at regions of contact to other subspecies groups (in Amur, Kirghizia–Kazakhstan, and Iran) show divergence from central population by nuclear and mitochondrial markers. In Amur, gene flow from minor group could be detected based on the existence of private minor alleles in the major population. In Kirghizia and Kazakhstan, the bokharensis and major groups share almost all the microsatellite alleles detected though frequencies differ. In Iran, three geographically close populations are distinct according to the mitochondrial sequences but also indications of present or recent admixture is detected. Populations, which have expanded to regions previously unoccupied by the species (northern UK and Finland), show divergence only by one of the markers. The variability in molecular differentiation may be due to dissimilar expansions, depending on whether the colonized regions have previously been occupied by another subspecies or not, on the amount of colonizing birds, and on the amount of past and present gene flow.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 201–210.     

Species limits and phylogeography of North American cricket frogs (Acris: Hylidae)

Cricket frogs are widely distributed across the eastern United States and two species, the northern cricket frog (Acris crepitans) and the southern cricket frog (A. gryllus) are currently recognized. We generated a phylogenetic hypothesis for Acris using fragments of nuclear and mitochondrial genes in separate and combined phylogenetic analyses. We also used distance methods and fixation indices to evaluate species limits within the genus and the validity of currently recognized subspecies of A. crepitans. The distributions of existing A. crepitans subspecies, defined by morphology and call types, do not match the distributions of evolutionary lineages recovered using our genetic data. We discuss a scenario of call evolution to explain this disparity. We also recovered distinct phylogeographic groups within A. crepitans and A. gryllus that are congruent with other codistributed taxa. Under a lineage-based species concept, we recognize Acris blanchardi as a distinct species. The importance of this revised taxonomy is discussed in light of the dramatic declines in A. blanchardi across the northern and western portions of its range.     

The great tit (Parus major) – a misclassified ring species

The great tit (Parus major) has been considered to be the most typical example of an avian ring species. The terminal taxa of the ring (major and minor sectors) are supposed to be reproductively isolated in a zone of secondary contact in the middle Amur valley, Siberia. Our study combines molecular markers (cytochrome‐b), bioacoustic analyses and morphological characters to judge the ring species status of the great tit complex. Despite a notable percentage of intermediately coloured birds in the mixed population of middle Amur, a lack of mitochondrial introgression between the major and minor sectors and a small number of true hybrids among voucher specimens from this area suggest at least a partial reproductive barrier between both sectors. In contrast, variation of morphological and especially acoustic characters along the ring‐shaped area and the phylogenetic structure of the P. major group do not match the ring species concept. Bioacoustic and molecular data (cytochrome‐b sequences) reveal two large and closely related subspecies blocks, the sectors major and bokharensis in the Western Palaearctic and central Asia, and the sectors minor and cinereus in the Eastern Palaearctic and South‐east Asia, respectively. The two western sectors diverged only recently (0.5 Mya) and they were separated from the eastern group by Pleistocene events about 1.5 Mya. Songs from allopatric regions of the two subspecies blocks differ distinctly in frequency parameters and element composition. In the area of secondary contact, males of all phenotypes share the same frequency range of song, close to the range of the typical minor song. Hybrids and major males sing mixed repertoires of typical major and minor strophe types as well as mixed strophes. In contrast, phenotypic minor males display only pure minor strophes. Differences in mate choice and mating success based on repertoire size are believed to uphold the reproductive barrier between major and minor birds in the area of sympatry. Taxonomic consequences suggest three separate species in the Parus major complex: Parus major s.s. (including the very closely related bokharensis sector), Parus minor and Parus cinereus. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 86 , 153–174.     

Speciation in chestnut-shouldered fairy-wrens (Malurus spp.) and rapid phenotypic divergence in variegated fairy-wrens (Malurus lamberti): a multilocus approach

The chestnut-shouldered fairy-wrens comprise a subgroup of four species in the genus Malurus (Passeriformes: Maluridae). Collectively, they are widespread across the Australian continent but phenotypic variation is strongly structured geographically in just one species, M. lamberti. Earlier phylogenetic analyses of this group have been limited to one or two individuals for each species and have not represented all currently recognised subspecies of M. lamberti. Historically, the taxonomy and nomenclature of the M. lamberti complex has been debated, in part because of morphological similarities among its subspecies and another member of the group, M. amabilis. We reconstructed the phylogeny of all four species of chestnut-shouldered fairy-wrens including all four subspecies of M. lamberti using a mitochondrial gene (ND2), five anonymous nuclear loci and three nuclear introns. Phylogenetic analysis of the mitochondrial ND2 gene nests M. amabilis within M. lamberti rendering the latter paraphyletic. Individual nuclear gene trees failed to reliably resolve each of the species boundaries or the phylogenetic relationships found in the mtDNA tree. When combined, however, a strongly supported overall topology was resolved supporting the monophyly of M. lamberti and its sister species relationship to M. amabilis. Current subspecific taxonomy of M. lamberti was not concordant with all evolutionary lineages of M. lamberti, nominotypical M. l. lamberti being the only subspecies recovered as a monophyletic group from mtDNA. Some genetic structuring is evident and potential barriers to gene flow are discussed.     

Systematics and evolutionary relationships of the mountain lizard Liolaemus monticola (Liolaemini): how morphological and molecular evidence contributes to reveal hidden species diversity

The delimitation of species is a major issue in systematic biology and has been a re-emerging discipline in the last decade. A number of studies have shown that the use of multiple data sets is critical for the identification of cryptic species, particularly in groups with complex evolutionary histories. Liolaemus monticola is a montane lizard species distributed in central Chile (32°–42°S), with four described subspecies in a latitudinal gradient from north to south: L. m. monticola , L. m. chillanensis , L. monticola ssp. and L. m. villaricensis . In order to test the systematic status and phylogenetic relationships of the taxa included in the L. monticola group, we analysed morphological (morphometric and meristic) and molecular (allozyme and mitochondrial DNA) data sets. The results of the morphological analyses showed that meristic variables correctly assigned individuals with higher accuracy than did morphometric characters. The results of the analyses of allozyme data revealed eight diagnostic loci that are evidence for significant differences among the four L. monticola subspecies. Phylogenetic analyses with mitochondrial DNA data, including additional species, showed that the L. monticola group is polyphyletic. We postulate that the four current subspecies represent independent evolutionary lineages and must be raised to the specific level as L. monticola , L. chillanensis and L. villaricensis . The taxonomic status of the unnamed L. monticola ssp. remains unresolved, although we provide a preliminary proposal.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 635–650.     

Genetic variation of complete mitochondrial genome sequences of the Sumatran rhinoceros (<Emphasis Type="Italic">Dicerorhinus sumatrensis</Emphasis>)

The Sumatran rhinoceros (Dicerorhinus sumatrensis) is the smallest and one of the most endangered rhinoceros species, with less than 100 individuals estimated to live in the wild. It was originally divided into three subspecies but only two have survived, D. sumatrensis sumatrensis (Sumatran subspecies), and D. s. harrissoni (Bornean). Questions regarding whether populations of the Sumatran rhinoceros should be treated as different management units to preserve genetic diversity have been raised, particularly in light of its severe decline in the wild and low breeding success in captivity. This work aims to characterize genetic differentiation between Sumatran rhinoceros subspecies using complete mitochondrial genomes, in order to unravel their maternal evolutionary history and evaluate their status as separate management units. We identified three major phylogenetic groups with moderate genetic differentiation: two distinct haplogroups comprising individuals from both the Malay Peninsula and Sumatra, and a third group from Borneo. Estimates of divergence time indicate that the most recent common ancestor of the Sumatran rhinoceros occurred approximately 360,000 years ago. The three mitochondrial haplogroups showed a common divergence time about 80,000 years ago corresponding with a major biogeographic event in the Sundaland region. Patterns of mitochondrial genetic differentiation may suggest considering Sumatran rhinoceros subspecies as different conservation units. However, the management of subspecies as part of a metapopulation may appear as the last resource to save this species from extinction, imposing a conservation dilemma.     

Introgressive hybridization in fishes: the biochemical evidence

Biochemical methods can detect variation at individual genetic loci, making possible the direct assessment of natural hybridization and introgression between fish populations. Protein electro-phoresis has been used to confirm and extend knowledge of many situations where species hybrids have been detected by morphological analyses. New cases of natural hybridization, including some at the subspecies level, have also been identified. Biochemical studies have provided the first conclusive evidence of natural post F₁ hybrids and of introgression between fish taxa. The strongest cases for introgression have used a combined analysis of nuclear protein genes and taxaspecific maternally inherited mitochondrial DNA variation. Information on the significance of introgression as a source of gene flow between taxa, particularly below the species level where sympatric subspecies and sibling species are involved, should expand in the future as the numbers and types of nuclear and mitochondrial DNA loci which can be assayed for variation increase. The full importance of introgressive hybridization in speciation may then be understood.     

Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds

A fragment of the mitochondrial cytochrome b gene of avian malaria (genera Haemoproteus and Plasmodium) was amplified from blood samples of 12 species of passerine birds from the genera Acrocephalus, Phylloscopus and Parus. By sequencing 478 nucleotides of the obtained fragments, we found 17 different mitochondrial haplotypes of Haemoproteus or Plasmodium among the 12 bird species investigated. Only one out of the 17 haplotypes was found in more than one host species, this exception being a haplotype detected in both blue tits (Parus caeruleus) and great tits (Parus major). The phylogenetic tree which was constructed grouped the sequences into two clades, most probably representing Haemoproteus and Plasmodium, respectively. We found two to four different parasite mitochondrial DNA (mtDNA) haplotypes in four bird species. The phylogenetic tree obtained from the mtDNA of the parasites matched the phylogenetic tree of the bird hosts poorly. For example, the two tit species and the willow warbler (Phylloscopus trochilus) carried parasites differing by only 0.6% sequence divergence, suggesting that Haemoproteus shift both between species within the same genus and also between species in different families. Hence, host shifts seem to have occurred repeatedly in this parasite host system. We discuss this in terms of the possible evolutionary consequences for these bird species.     

A molecular phylogenetic analysis of invasive and ornamental brooms and their relationships within the Genistoid legumes

The Cytisus-Genista complex includes species that have become invasive following introduction into new geographic ranges as ornamental shrubs. Despite their impacts, the evolutionary relationships among invasives, ornamentals, and native-range species have never been investigated. Our objective was to examine relationships within the Cytisus-Genista complex to determine (1) the taxonomic identity of invasive "French broom" and ornamental "sweet broom" and (2) whether "sweet broom" contributes to "French broom" populations directly or via hybridization. We used sequence data from chloroplast and nuclear regions to gain insight into evolutionary origins and to confirm taxonomic status. Our phylogenetic analyses suggest a complex evolutionary history that includes hybridization events. Placement of invasive and ornamental individuals within the Cytisus-Genista complex resolves taxonomic uncertainty in these groups, as our phylogenetic analyses recovered separate "French broom" and "sweet broom" clades within the G. monspessulana clade in the genus Genista. Extensive cloning and sequencing of the ITS region revealed that, although the majority of invasive "French broom" in California is Genista monspessulana, hybridization with individuals from the ornamental "sweet broom" clade likely occurs in populations throughout the state.     

Genetic variation of the Siberian tit Parus cinctus populations at the regional level: a mitochondrial sequence analysis

We studied the matrilinear genetic structure of the Siberian tit Parus cinctus by sequencing 911 bp of the mitochondrial control region of 56 birds from Fennoscandia and 3 from Yakutia, central Siberia, representing subspecies P. c. lapponicus and P. c. cinctus , respectively. One major haplotype comprised 35.7% of all birds and was present in all Fennoscandian populations. Sequence variation of 5 museum specimens from Norway fitted with the pattern of the present-day birds. The nucleotide diversity was 0.00205±0.00025 in the Fennoscandian population and no population structuring was detected. The star-like phylogeny suggests a recent expansion of the population size in the evolutionary time scale. A modern decline of the population size from 200 000 pairs to 50 000 pairs in Finland has resulted from cutting and fragmentation of old-growth forests, but the effects of this could not yet be detected in the mtDNA pattern. However, the nucleotide diversity differed among populations being the highest at Kuusamo, close to the Russian border. Conceivably, the gene flow maintained by the substantial migration of Siberian tits is sufficient to prevent differentiation of local populations in Fennoscandia. Presumably the large conservation areas in NE Finland and on the Russian side of the border contribute to the high genetic variation observed in the Kuusamo population. Comparison of the mtDNA phylogeny of the Siberian tit with the phylogenies of the great tit, the blue tit and the willow tit showed that the Siberian tit and some other non-migratory species of the foliage gleaning guild share similar post glacial histories in the western palaearctic.     

Phylogenetic analysis under reticulate evolution

The usual assumption that species have evolved from a common ancestor by a simple branching process--where each branch is genetically isolated--has been challenged by the observation of frequent hybridization between species in natural populations. In fact, most plant species are thought to have hybrid origins. This reticulate pattern of species evolution has posed problems in the definition of speciation and in phylogenetic reconstruction, especially when molecular data are used. As a result, hybridization has been largely treated as an evolutionary accident or statistical error in phylogenetic analysis. In this paper, I explicitly incorporate hybridization as an evolutionary occurrence and then conduct phylogenetic reconstruction. I first examine the reticulate evolution under a pure drift model, and then extend the theory to fit a mutation model. A least-squares method is developed for reconstructing a reticulate phylogeny using gene frequency data. The efficacy of the method under the pure drift model is verified via Monte Carlo simulations.     

Gene trees and species trees – mutual influences and interdependences of population genetics and systematics

Both population genetics and systematics are core disciplines of evolutionary biology. While systematics deals with genealogical relationships among taxa, population genetics has mainly been based on allele frequencies and the distribution of genetic variants whose genealogical relations could for a long time, due mainly to methodological constraints, not be inferred. The advent of mitochondrial DNA analyses and modern sequencing techniques in the 1970s revolutionized evolutionary genetic studies and gave rise to molecular phylogenetics. In the wake of this new development systematic approaches and principles were incorporated into intraspecific studies at the population level, e.g. the concept of monophyly which is used to delineate evolutionarily significant units in conservation biology. A new discipline combining phylogenetic analyses of genetic lineages with their geographic distribution ('phylogeography') was introduced as an explicit synthesis of population genetics and systematics. On the other hand, it has increasingly become obvious that discordances between gene trees and species trees not only result from spurious data sets or methodological flaws in phylogenetic analyses, but that they often reflect real population genetic processes such as lineage sorting or hybridization. These processes have to be taken into account when evaluating the reliability of gene trees to avoid wrong phylogenetic conclusions. The present review focuses on the phenomenon of non-phylogenetic sorting of ancestral polymorphisms, its probability and its consequences for molecular systematics.     

What we don't know about great ape variation

The patterning of intraspecific variation among the great apes is proving more complex than has been recognized previously. The great ape species, as currently defined, may include markedly different subspecies, alternatively, the majority of intraspeclflc variation may be observed at the populational level within a single subspecies. Recent studies have raised a number of questions about great ape evolutionary biology. How many species of living great apes exist? What was the original dietary adaptation of gorillas? How should we define male orang-utan adulthood?     

The lesser wanderer butterfly, Danaus petilia (Stoll 1790) stat. rev. (Lepidoptera: Danainae), reinstated as a species

Abstract  The lesser wanderer butterfly, Danaus ( Anosia ) chrysippus petilia (Stoll) (Lepidoptera: Danainae), has been treated as a subspecies for the last 100 years. New mitochondrial DNA sequence data for D. petilia , in conjunction with allozyme, structural, morphometric and pattern characters, constitute a compelling case for its specific rank. The holotype of D. petilia has never been located and, as the type location is uncertain, a neotype is designated. Fresh material was collected and examined for this project. Danaus petilia and D. chrysippus have been separated at Lydekker's Line for an estimated 1.1 million years, and they remain interfertile. However, as an allopatric taxon, diagnosable from D. chrysippus , D. petilia merits specific status under the phylogenetic species concept. The following pairs of D. chrysippus subspecies are considered to be synonyms, the first member of each pair having priority: chrysippus  +  aegyptius (subspecies), klugii  +  infumata (hybrid phenotypes) and orientis  + liboria (subspecies).