Conservation genomics and systematics of a near-extinct island radiation.

Conservation benefits from incorporating genomics to explore the impacts of population declines, inbreeding, loss of genetic variation and hybridization. Here we use the near-extinct Mariana Islands reedwarbler radiation to showcase how ancient DNA approaches can allow insights into the population dynamics of extinct species and threatened populations for which historical museum specimens or material with low DNA yield (e.g., scats, feathers) are the only sources for DNA. Despite their having paraphyletic mitochondrial DNA (mtDNA), nuclear single nucleotide polymorphisms (SNPs) support the distinctiveness of critically endangered Acrocephalus hiwae and the other three species in the radiation that went extinct between the 1960s and 1990s. Two extinct species, A. yamashinae and A. luscinius, were deeply divergent from each other and from a third less differentiated lineage containing A. hiwae and extinct A. nijoi. Both mtDNA and SNPs suggest that the two isolated populations of A. hiwae from Saipan and Alamagan Islands are sufficiently distinct to warrant subspecies recognition and separate conservation management. We detected no significant differences in genetic diversity or inbreeding between Saipan and Alamagan, nor strong signatures of geographical structuring within either island. However, the implications of possible signatures of inbreeding in both Saipan and Alamagan, and long-term population declines in A. hiwae that pre-date modern anthropogenic threats require further study with denser population sampling. Our study highlights the value that conservation genomics studies of island radiations have as windows onto the possible future for the world's biota as climate change and habitat destruction increasingly fragment their ranges and contribute to rapid declines in population abundances.

Inter- and intra-archipelago dynamics of population structure and gene flow in a Polynesian bird.

Islands are separated by natural barriers that prevent gene flow between terrestrial populations and promote allopatric diversification. Birds in the South Pacific are an excellent model to explore the interplay between isolation and gene flow due to the region's numerous archipelagos and well-characterized avian communities. The wattled honeyeater complex (Foulehaio spp.) comprises three allopatric species that are widespread and common across Fiji, Tonga, Samoa, and Wallis and Futuna. Here, we explored patterns of diversification within and among these lineages using genomic and morphometric data. We found support for three clades of Foulehaio corresponding to three recognized species. Within F. carunculatus, population genetic analyses identified nine major lineages, most of which were composed of sub-lineages that aligned nearly perfectly to individual island populations. Despite genetic structure and great geographic distance between populations, we found low levels of gene flow between populations in adjacent archipelagos. Additionally, body size of F. carunculatus varied randomly with respect to evolutionary history (as Ernst Mayr predicted), but correlated negatively with island size, consistent with the island rule. Our findings support a hypothesis that widespread taxa can show population structure between immediately adjacent islands, and likely represent many independent lineages loosely connected by gene flow.

Near-complete phylogeny and taxonomic revision of the world's babblers (Aves: Passeriformes).

The babblers are a diverse group of passerine birds comprising 452 species. The group was long regarded as a "scrap basket" in taxonomic classification schemes. Although several studies have assessed the phylogenetic relationships for subsets of babblers during the past two decades, a comprehensive phylogeny of this group has been lacking. In this study, we used five mitochondrial and seven nuclear loci to generate a dated phylogeny for babblers. This phylogeny includes 402 species (ca. 89% of the overall clade) from 75 genera (97%) and all five currently recognized families, providing a robust basis for taxonomic revision. Our phylogeny supports seven major clades and reveals several non-monophyletic genera. Divergence time estimates indicate that the seven major clades diverged around the same time (18-20 million years ago, Ma) in the early Miocene. We use the phylogeny in a consistent way to propose a new taxonomy, with seven families and 64 genera of babblers, and a new linear sequence of names.

Comprehensive molecular phylogeny of barn owls and relatives (Family: Tytonidae), and their six major Pleistocene radiations.

The owl family Tytonidae comprises two genera: Phodilus, limited to the forests of central Africa and South-East Asia, and the ubiquitous Tyto. The genus Tyto is majorly represented by the cosmopolitan Common Barn Owl group, with more than 30 subspecies worldwide. Discrete differences in body size and plumage colouration have led to the classification of this family into many species and subspecies, but the taxonomic status and phylogenetic relationships between taxa remain unclear, and in some groups controversial. Although several previous studies attempted to resolve this problem, they have been limited in their taxonomic and geographical coverage, or have relied on restricted molecular evidence and low sample sizes. Based on the most comprehensive sampling to date (16 out of 17 Tyto species, and one out of three Phodilus species), a multi-locus approach using seven mitochondrial and two nuclear markers, and taking advantage of field data and museum collections available worldwide, our main questions in this study were: (1) what are the phylogenetic relationships and classification status of the whole family; (2) when and where did the most important speciation events occur? We confirm that the Common Barn Owl, Tyto alba is divided into three main evolutionary units: the American Barn Owl, T. furcata; the Western Barn Owl, T. alba; and the Eastern Barn Owl, T. javanica, and suggest a Late Miocene (ca. 6 mya) Australasian and African origin of the group. Our results are supported by fossil age information, given that the most recent common ancestor between the Tytonidae genera Phodilus and Tyto was probably from the Oligocene (ca. 28 mya) of Australasia. We finally reveal six major Pleistocene radiations of Tyto, all resulting in wide-range distributions.

Comprehensive molecular phylogeny of the grassbirds and allies (Locustellidae) reveals extensive non-monophyly of traditional genera, and a proposal for a new classification.

The widespread Old World avian family Locustellidae ('grassbirds and allies') comprises 62 extant species in 11 genera. In the present study, we used one mitochondrial and, for most species, four nuclear loci to infer the phylogeny of this family. We analysed 59 species, including the five previously unsampled genera plus two genera that had not before been analysed in a densely sampled dataset. This study revealed extensive disagreement with current taxonomy; the genera Bradypterus, Locustella, Megalurus, Megalurulus and Schoenicola were all found to be non-monophyletic. Non-monophyly was particularly pronounced for Megalurus, which was widely scattered across the tree. Three of the five monotypic genera (Amphilais, Buettikoferella and Malia) were nested within other genera; one monotypic genus (Chaetornis) formed a clade with one of the two species of Schoenicola; whereas the position of the fifth monotypic genus (Elaphrornis) was unresolved. Robsonius was confirmed as sister to the other genera. We propose a phylogenetically informed revision of genus-level taxonomy, including one new generic name. Finally, we highlight several non-monophyletic species complexes and deep intra-species divergences that point to conflict in taxonomy and suggest an underestimation of current species diversity in this group.

Phylogeny and biogeography of the imperial pigeons (Aves: Columbidae) in the Pacific Ocean.

We reconstruct the phylogeny of imperial pigeons (genus Ducula) using mitochondrial and nuclear sequence data. We evaluate the most likely biogeographic scenario for the evolution of this group that colonized many islands of the Pacific Ocean. The divergence time analysis suggests that the basal divergences within Ducula occurred more recently than in the fruit doves (genus Ptilinopus), a group that is also well diversified in Oceania. The imperial pigeons colonized the Melanesian region several times independently, and the diversification within this region led to several species in sympatry, in particular in the Bismarck archipelago. Central Polynesia was also colonized several times, first by a lineage during the Miocene that led to the large D. latrans, sister to the New Caledonian endemic D. goliath, then more recently by the widespread D. pacifica, during the Pleistocene. The phylogenetic pattern obtained with the extant Ducula species showed that the Eastern Polynesian endemics do not form a monophyletic group, with the Pacific Imperial Pigeon D. pacifica sister species with good support to the Polynesian Imperial Pigeon D. aurorae. However, the impact of recent anthropic extinctions has been important for the imperial pigeons, more than for the smaller fruit doves, suggesting that several Ducula lineages might be missing today.

Phylogeny and biogeography of the fruit doves (Aves: Columbidae).

We reconstruct the phylogeny of fruit doves (genus Ptilinopus) and allies with a dense sampling that includes almost all species, based on mitochondrial and nuclear sequence data. We evaluate the most likely biogeographic scenario for the evolution of this group that colonized many islands of the Pacific Ocean. We also investigate the evolution of one of the main plumage character of fruit doves (the color of the crown), and we propose several revisions of the group's systematics. All Ptilinopus taxa formed a monophyletic group that includes two morphologically distinct genera, Alectroenas and Drepanoptila, confirming a previous result found with less species and genes. The divergence time analysis suggests that the basal divergences within Ptilinopus dated to the Early Oligocene, and the biogeographic analysis indicates that fruit doves originated most probably from the proto New Guinea region. The earliest dispersals from the New Guinea region to Oceania occurred with the colonization of New Caledonia and Fiji. A large group of Polynesian species (Central and Eastern), as well as the three taxa found in Micronesia and four species from the Guinean-Moluccan region, form the "purpuratus" clade, the largest diversification of fruit doves within Oceania, which also has a New Guinean origin. However, the eastbound colonization of fruit doves was not associated with a significant increase of their diversification rate. Overall, the Melanesian region did not act as a cradle for fruit doves, in contrast to the New Guinea region which is found as the ancestral area for several nodes within the phylogeny.

Molecular phylogenetic reconstructions identify East Asia as the cradle for the evolution of the cosmopolitan genus Myotis (Mammalia, Chiroptera).

Sequences of the mitochondrial cytochrome b (1140 bp) and nuclear Rag 2 (1148 bp) genes were used to assess the evolutionary history of the cosmopolitan bat genus Myotis, based on a worldwide sampling of over 88 named species plus 7 species with uncertain nomenclature. Phylogenetic reconstructions of this comprehensive taxon sampling show that most radiation of species occurred independently within each biogeographic region. Our molecular study supports an early divergence of species from the New World, where all Nearctic and Neotropical species plus a lineage from the Palaearctic constitute a monophyletic clade, sister to the remaining Old World taxa. The major Old World clade includes all remaining Eurasian taxa, most Oriental species, one Oceanian, and all Ethiopian species. Another lineage, including M. latirostris from Taiwan, appears at the base of these two major biogeographic clades and, because it bears nyctalodont molars, could be considered as a distinct genus. However, this molar configuration is also found in crown-group species, indicating that these dental characters are variable in the genus Myotis and may confound interpretation of the fossil record. Molecular datings suggest an origin of all recent Myotis in the early Miocene (about 21MYA with 95% highest posterior density interval 23-20MYA). This period was characterized by a global climatic cooling that reduced the availability of tropical habitats and favoured the development of more temperate vegetation. This sharp climatic change might have triggered the evolution of Myotis in the Northern continents, because Myotis ancestors seem to have been well adapted and successful in such temperate habitats. Ancestral area reconstructions based on the molecular phylogeny suggest that the eastern portion of the Asian continent was an important center of origin for the early diversification of all Myotis lineages, and involved relatively few subsequent transcontinental range expansions.

Determinants of haemosporidian single- and co-infection risks in western palearctic birds.

Understanding the drivers of infection risk helps us to detect the most at-risk species in a community and identify species whose intrinsic characteristics could act as potential reservoirs of pathogens. This knowledge is crucial if we are to predict the emergence and evolution of infectious diseases. To date, most studies have only focused on infections caused by a single parasite, leaving out co-infections. Yet, co-infections are of paramount importance in understanding the ecology and evolution of host-parasite interactions due to the wide range of effects they can have on host fitness and on the evolutionary trajectories of parasites. Here, we used a multinomial Bayesian phylogenetic modelling framework to explore the extent to which bird ecology and phylogeny impact the probability of being infected by one genus (hereafter single infection) or by multiple genera (hereafter co-infection) of haemosporidian parasites. We show that while nesting and migration behaviours influenced both the probability of being single- and co-infected, species position along the slow-fast life-history continuum and geographic range size were only pertinent in explaining variation in co-infection risk. We also found evidence for a phylogenetic conservatism regarding both single- and co-infections, indicating that phylogenetically related bird species tend to have similar infection patterns. This phylogenetic signal was four times stronger for co-infections than for single infections, suggesting that co-infections may act as a stronger selective pressure than single infections. Overall, our study underscores the combined influence of hosts' evolutionary history and attributes in determining infection risk in avian host communities. These results also suggest that co-infection risk might be under stronger deterministic control than single infection risk, potentially paving the way toward a better understanding of the emergence and evolution of infectious diseases.

Influence of quaternary sea-level variations on a land bird endemic to Pacific atolls.

Little is known about the effect of quaternary climate variations on organisms that inhabited carbonate islands of the Pacific Ocean, although it has been suggested that one or several uplifted islands provided shelter for terrestrial birds when sea-level reached its highest. To test this hypothesis, we investigated the history of colonization of the Tuamotu reed-warbler (Acrocephalus atyphus) in southeastern Polynesia, and found high genetic structure between the populations of three elevated carbonate islands. Estimates of time since divergence support the hypothesis that these islands acted as refugia during the last interglacial maximum. These findings are particularly important for defining conservation priorities on atolls that endure the current trend of sea-level rise owing to global warming.

Origins, identification and type status of two early specimens of Society Kingfisher Todiramphus veneratus (J. F. Gmelin, 1788) (Aves: Coraciiformes, Alcedinidae).

We re-examined the putative type specimen of Society Kingfisher Todiramphus veneratus (J. F. Gmelin, 1788) in the Naturhistorisches Museum Wien (NMW 50.633) and conclude based on plumage that it represents the taxon from Moorea, T. veneratus youngi Sharpe, 1892, rather than nominate T. veneratus veneratus from Tahiti. X-rays reveal that it was prepared using techniques common in the late 18th century, and that its preparation style matches that of other specimens collected during Cook's three voyages. NMW 50.633 has been assumed to be the one, or one of a number of, specimen(s) used by Latham to describe and illustrate his 'Venerated Kingfisher' (present-day Society Kingfisher), which was the basis of the later valid introduction of the name Alcedo venerata by J. F. Gmelin. However, whereas the description and an unpublished illustration in Latham's archives agree closely with veneratus from Tahiti, NMW 50.633 appears to represent Moorea youngi. While this finding does not compromise the definition of Society Kingfisher veneratus, it leaves it without a safely identified type specimen. We also examined a Moorea specimen in the National Museums Liverpool (LIVCM D2366) that is almost as old as NMW 50.633, but which X-rays suggest had a different origin than NMW 50.633.

Rapid diversification and secondary sympatry in Australo-Pacific kingfishers (Aves: Alcedinidae: Todiramphus).

Todiramphus chloris is the most widely distributed of the Pacific's 'great speciators'. Its 50 subspecies constitute a species complex that is distributed over 16 000 km from the Red Sea to Polynesia. We present, to our knowledge, the first comprehensive molecular phylogeny of this enigmatic radiation of kingfishers. Ten Pacific Todiramphus species are embedded within the T. chloris complex, rendering it paraphyletic. Among these is a radiation of five species from the remote islands of Eastern Polynesian, as well as the widespread migratory taxon, Todiramphus sanctus. Our results offer strong support that Pacific Todiramphus, including T. chloris, underwent an extensive range expansion and diversification less than 1 Ma. Multiple instances of secondary sympatry have accumulated in this group, despite its recent origin, including on Australia and oceanic islands in Palau, Vanuatu and the Solomon Islands. Significant ecomorphological and behavioural differences exist between secondarily sympatric lineages, which suggest that pre-mating isolating mechanisms were achieved rapidly during diversification. We found evidence for complex biogeographic patterns, including a novel phylogeographic break in the eastern Solomon Islands that separates a Northern Melanesian clade from Polynesian taxa. In light of our results, we discuss systematic relationships of Todiramphus and propose an updated taxonomy. This paper contributes to our understanding of avian diversification and assembly on islands, and to the systematics of a classically polytypic species complex.

What are African monarchs (Aves, Passeriformes)? A phylogenetic analysis of mitochondrial genes.

We address the phylogenetic relationships of ten passerine bird species representing the five presently supposed monarchine (family Monarchidae) genera (Terpsiphone, Hypothymis, Elminia, Trochocercus, Erythrocercus) from Asia and Africa, as well as three monarchs from Australasia, three representatives of the related genera Rhipidura and Dicrurus, and 20 representatives of 11 other oscine groups (including two Culicicapa flycatchers) and one sub-oscine, using two partial mitochondrial genes (cytochrome b and large sub-unit ribosomal 16S RNA). Molecular data corroborate ecological, ethological and morphological observations on the probable heterogeneity of Trochocercus and indicate that this genus is polyphyletic; two of its species are members of Monarchidae allied to Terpsiphone and Hypothymis; the others are more closely related to Elminia. Elminia is not a member of Monarchidae and is not related to any other sampled species, except Culicicapa. Erythrocercus is also outside the Monarchidae but inside a Sylvii-Pycnonotidae group. These results point once more to the need of a fully revised phylogeny of passerine birds.

Cryptic differentiation in the endemic micromoth Galagete darwini (Lepidoptera, Autostichidae) on Galápagos volcanoes.

To gain insight into the early stages of speciation, we reconstructed a DNA-based phylogeny, using combined mitochondrial (cytochrome c oxidase subunits I and II: 1008 bp) and nuclear (elongation factor 1-alpha and wingless: 1062 bp) markers of populations of the moth Galagete darwini endemic to the Galápagos, which belongs to an insular radiation similar in size to that of Darwin's finches. Adults of G. darwini were collected in the arid lowlands of 11 of the Galápagos Islands (Baltra, Española, Fernandina, Floreana, Isabela, Pinta, Pinzón, San Cristobal, Santa Cruz, Santiago and Seymour) and the humid highlands of a subset of 5 of them (Fernandina, Floreana, Isabela, Santa Cruz and Santiago). The combined phylogeographic analysis surprisingly revealed that G. darwini populations at higher elevation on the western islands (Fernandina, Isabela and Santiago) represent a distinct lineage from the one in the low arid zones of these same islands. This is the first reported case in the archipelago of genetic cryptic differentiation correlated with elevation on the western Galápagos volcanoes.

Molecular phylogeny and dating of an insular endemic moth radiation inferred from mitochondrial and nuclear genes: the genus Galagete (Lepidoptera: Autostichidae) of the Galapagos Islands.

Galagete is a genus of microlepidoptera including 12 nominate species endemic to the Galapagos Islands. In order to better understand the diversification of this endemic insular radiation, to unravel relationships among species and populations, and to get insight into the early stages of speciation, we developed a phylogenetic reconstruction based on the combined mitochondrial cytochrome oxidase I (555bp) and II (453bp), and the nuclear elongation factor-1alpha (711bp) and wingless (351bp) genes. Monophyly of the genus is strongly supported in the Bayesian and maximum likelihood analyses suggesting a single colonization event by a common ancestor. Two cases of paraphyly observed between species are hypothesized to represent imperfect species limits for G. espanolaensis nested within the G. turritella clade, and introgressive hybridization or lineage sorting in the case of the population of G. protozona from Santa Fe nested within the G. gnathodoxa clade. A geologically calibrated, relaxed molecular clock model was used for the first time to unravel the chronological sequence of an insular radiation. The first split occurring within the Galagete lineage on the archipelago is estimated at 3.3+/-0.4million years ago. The genus radiated relatively quickly in about 1.8million years, and gives an estimated speciation rate of 0.8 species per million years. Although the colonization scenario shows a stochastic dispersal pattern, the arrival of the ancestor and the diversification of the radiation coincide with the chronological emergence of the major islands.

Nuclear and mitochondrial sequence data reveal the major lineages of starlings, mynas and related taxa.

We investigated the phylogenetic relationships among the major lineages of the avian family Sturnidae and their placement within the Muscicapoidea clade using two nuclear (RAG-1 and myoglobin) and one mitochondrial gene (ND2). Among Muscicapoidea, we recovered three clades corresponding to the families Cinclidae, Muscicapidae and Sturnidae (sensu [Sibley, C.G., Monroe Jr., B.L., 1990. Distribution and Taxonomy of Birds of the World. Yale University Press, New Haven, CT]). Within the sturnoid lineage Mimini and Sturnini are sister groups, with Buphagus basal to them. We identified three major lineages of starlings: the Philippine endemic genus Rhabdornis, an Oriental-Australasian clade (genera Scissirostrum, Gracula, Mino, Ampeliceps, Sarcops, Aplonis), and an Afrotropical-Palaearctic clade (all African taxa, Sturnus and Acridotheres). We discuss the biogeographic implications of our findings and suggest an Asiatic origin for this family. The congruence between the age of major clades, estimated by NPRS, and palaeoclimatic data present evidence for the role of climatic changes in shaping present day distribution of the group.

Assessing the passerine "Tapestry": phylogenetic relationships of the Muscicapoidea inferred from nuclear DNA sequences.

This study presents new comparative sequence data from the nuclear RAG-1 gene for an increased taxon sample in order to investigate phylogenetic relationships among a diverse songbird superfamily, the Muscicapoidea, which has variously included the waxwings, silky flycatchers, Palm Chat, dippers, starlings, mockingbirds, thrushes, chats, and Old World flycatchers. At the same time, our results provide a test of the often-cited relationships inferred from the phenetic studies of Sibley and Ahlquist [Phylogeny and Classification of Birds: A Study in Molecular Evolution. Yale University Press, New Haven, 1990] using DNA hybridization distances. Nuclear DNA sequences confirm the monophyly of the "core muscicapoid" group, as defined by Barker et al. [Proc. R. Soc. Lond. B 269 (2002) 295] and also support the sister-group relationship of the Sturnidae and Mimidae, on the one hand, and the large-bodied thrushes (Turdini)+the Old World flycatchers and robins, on the other. The results of the phylogenetic analysis allow preliminary inferences about muscicapoid biogeographic history.

Phylogeny and diversification of the largest avian radiation.

The order Passeriformes ("perching birds") comprises extant species diversity comparable to that of living mammals. For over a decade, a single phylogenetic hypothesis based on DNA-DNA hybridization has provided the primary framework for numerous comparative analyses of passerine ecological and behavioral evolution and for tests of the causal factors accounting for rapid radiations within the group. We report here a strongly supported phylogenetic tree based on two single-copy nuclear gene sequences for the most complete sampling of passerine families to date. This tree is incongruent with that derived from DNA-DNA hybridization, with half of the nodes from the latter in conflict and over a third of the conflicts significant as assessed under maximum likelihood. Our historical framework suggests multiple waves of passerine dispersal from Australasia into Eurasia, Africa, and the New World, commencing as early as the Eocene, essentially reversing the classical scenario of oscine biogeography. The revised history implied by these data will require reassessment of comparative analyses of passerine diversification and adaptation.