Lovette, I .J. and E. Bermingham. 2002. What is a wood-warbler? A molecular characterization of a monophyletic Parulidae. Auk 119, 695-714.

Abstract: The wood-warblers (family Parulidae) fall within a radiation of passerine birds commonly known as the New World nine-primaried oscines. Defining familial relationships within that radiation has previously been challenging because of its extremely high diversity, a paucity of phylogenetically informative morphological characters, and an apparent high rate of cladogenesis early in the radiation's history. Here, analyses of mitochondrial and nuclear DNA sequences demonstrate that the 25 extant genera traditionally placed in the Parulidae do not form a monophyletic group. Instead, all reconstructions identify a well-resolved clade of 19 genera (Vermivora, Parula, Dendroica, Catharopeza, Mniotilta, Setophaga, Protonotaria, Helmitheros, Limnothlypis, Seiurus, Oporornis, Geothlypis, Wilsonia, Cardellina, Ergaticus, Myioborus, Euthlypis, Basileuterus, and Phaeothlypis ) that are all morphologically typical wood-warblers traditionally placed in the Parulidae. Six genera traditionally assigned to the Parulidae-Microligea, Teretistris, Zeledonia, Icteria, Granatellus, and Xenoligea -fall outside this highly supported clade in all mtDNA-based and nuclear DNA-based reconstructions, and each is probably more closely allied to taxa traditionally placed in other nine-primaried oscine families. The long, well-supported, and independently confirmed internode at the base of this wood-warbler clade provides the opportunity to define a monophyletic Parulidae using several complementary molecular phylogenetic criteria. Support for those relationships comes from reconstructions based on a range of nucleotide-intensive (from 894 to 3,638 nucleotides per taxon) and taxon-intensive (45 to 128 species) analyses of mtDNA sequences, as well as independent reconstructions based on nucleotide substitutions in the nuclear-encoded c-mos gene. Furthermore, the 19 typical wood-warbler genera share a synapomorphic one-codon c-mos deletion not found in other passerines. At a slightly deeper phylogenetic level, our mtDNA-based reconstructions are consistent with previous morphologic and genetic studies in suggesting that many nine-primaried oscine taxa have unanticipated affinities, that many lineages arose during an early and explosive period of cladogenesis, and that the generation of a robust nine-primaried oscine phylogeny will require robust taxonomic sampling and extensive phylogenetic information.

Kimura, M., S. M. Clegg, I. J. Lovette, K. R. Holder, D. J. Girman, B. Mila, P. Wade, and T. B.Smith. 2002. Phylogeographical approaches to assessing demographic connectivity between breeding and overwintering regions in a Nearctic-Neotropical warbler (Wilsonia pusilla). Molecular Ecology 9, 1605-1616.

Abstract: We characterized the pattern and magnitude of phylogeographical variation among breeding populations of a long-distance migratory bird, the Wilson's warbler (Wilsonia pusilla), and used this information to assess the utility of mtDNA markers for assaying demographic connectivity between breeding and overwintering regions. We found a complex pattern of population differentiation in mitochondrial DNA (mtDNA) variation among populations across the breeding range. Individuals from eastern North America were differentiated from western individuals and the eastern haplotypes formed a distinct, well-supported cluster. The more diverse western group contained haplotype clusters with significant geographical structuring, but there was also broad mixing of haplotype groups such that no haplotype groups were population specific and the predominance of rare haplotypes limited the utility of frequency-based assignment techniques. Nonetheless, the existence of geographically diagnosable eastern vs. western haplotypes enabled us to characterize the distribution of these two groups across 14 overwintering locations. Western haplotypes were present at much higher frequencies than eastern haplotypes at most overwintering sites. Application of this mtDNA-based method of linking breeding and overwintering populations on a finer geographical scale was precluded by the absence of population-specific markers and by insufficient haplotype sorting among western breeding populations. Our results suggest that because migratory species such as the Wilson's warbler likely experienced extensive gene flow among regional breeding populations, molecular markers will have the greatest utility for characterizing breeding-overwintering connectivity at a broad geographical scale.

Lovette, I. J., E. Bermingham, and R. E. Ricklefs. 2001. Clade-specific morphological diversification and adaptive radiation in Hawaiian songbirds. Proceedings of the Royal Society of London: Biological Sciences 269:37-42.

Abstract: The Hawaiian honeycreepers are a dramatic example of adaptive radiation but contrast with the four other songbird lineages that successfully colonized the Hawaiian archipelago and failed to undergo similar diversification. To explore the processes that produced the diversity dichotomy in this insular fauna, we compared clade age and morphologic diversity between the speciose honeycreepers and the comparatively depauperate Hawaiian thrushes. Mitochondrial-DNA-based genetic distances between these Hawaiian clades and their continental sister taxa indicate that the ancestral thrush colonized the Hawaiian Islands as early as the common ancestor of the honeycreepers. This similar timing of colonization indicates that the marked difference in diversity between the Hawaiian honeycreeper and thrush clades is unlikely to result from differences in these clades' tenures within the archipelago. If time cannot explain the contrasting diversities of these taxa, then an intrinsic, clade-specific trait may have fostered the honeycreeper radiation. Because the honeycreepers have diversified most dramatically in morphological characters related to resource utilization, we used principal components analyses of bill characters to compare the magnitudes of morphological variation in the ancestral clades from which the Hawaiian honeycreeper and thrush lineages are derived, the Carduelini and Turdinae respectively. Although the Carduelini share a more recent common ancestor and have a lower species diversity than the Turdinae, these finch-like relatives of the honeycreepers exhibit significantly greater variation in bill morphology than do the continental relatives of the Hawaiian thrushes. The higher magnitude of morphological variation in the non-Hawaiian Carduelini suggests that the honeycreepers fall within a clade exhibiting a generally high evolutionary flexibility in bill morphology. Accordingly, although the magnitude of bill variation among the honeycreepers is similar to that of the entire passerine radiation, this dramatic morphological radiation represents but an extreme manifestation of a general clade-specific ability to evolve novel morphologies.

Lovette, I. J., and E. Bermingham. 2001. A mitochondrial sequence-based phylogenetic analysis of Parula wood-warblers (Aves: Parulidae). Auk 118, 211-215.

Lovette, I. J., and E. Bermingham. 2000. C-mos variation in songbirds: Molecular evolution, phylogenetic implications, and comparisons with mitochondrial differentiation. Molecular Biology and Evolution 17, 1569-1577.

Abstract: Nucleotide sequences from the c-mos proto-oncogene have previously been used to reconstruct the phylogenetic relationships between distantly related vertebrate taxa. To explore c-mos variation at shallower levels of avian divergence, we compared c-mos sequences from representative passerine taxa that span a range of evolutionary differentiation, from basal passerine lineages to closely allied genera. Phylogenetic reconstructions based on these c-mos sequences recovered topologies congruent with previous DNA-DNA hybridization-based reconstructions, with many nodes receiving high support, as indicated by bootstrap and reliability values. One exception was the relationship of Acanthisitta to the remaining passerines, where the c-mos-based searches indicated a three-way polytomy involving the Acanthisitta lineage and the suboscine and oscine passerine clades. We also compared levels of c-mos and mitochondrial differentiation across eight oscine passerine taxa and found that c-mos nucleotide substitutions accumulate at a rate similar to that of transversion substitutions in mitochondrial protein-coding genes. These comparisons suggest that nuclear-encoded loci such as c-mos provide a temporal window of phylogenetic resolution that overlaps the temporal range where mitochondrial protein-coding sequences have their greatest utility and that c-mos substitutions and mtDNA transversions can serve as complementary, informative, and independent phylogenetic markers for the study of avian relationships.

Price, T., I. J. Lovette, E. Bermingham, L. Gibbs, and A. Richman. 2000. The imprint of history on two warbler adaptive radiations. American Naturalist 156, 354-367.

Abstract: The ecology of the component species of an adaptive radiation is likely to be influenced by the form of the founding ancestor to the radiation, its timing, and rates of speciation and extinction. These historical features complement environmental selection pressures. They imply that, if the history of the species' radiations are very different, ecological communities are unlikely to be completely convergent even when placed in identical environments. We compare the adaptive radiation of the Dendroica warblers of North America with that of the Phylloscopus warblers of Asia. We consider the ecology of the species in two localities where species' diversity is very high (New Hampshire, U.S.A., and Kashmir, India, respectively) and contrast the history of the two radiations on the basis of a molecular (mitochondrial cytochrome b) phylogeny. By comparison with the Phylloscopus, the Dendroica are on average larger and morphologically more similar to one another. Although there is some similarity between the Dendroica and Phylloscopus communities, they differ in foraging behavior and in associations of morphology with ecological variables. The Dendroica likely reflect an early Pliocene radiation and are two to four times younger than the Phylloscopus. They probably had a colorful sexually dichromatic ancestor, implicating sexual selection in the production of the many ecologically similar species. The Phylloscopus are much older and probably had a drab, monomorphic ancestor. Given the difference in ages of the two radiations, it is plausible that the close species' packing of the Dendroica warblers is a transient phenomenon. If this is the case, community structure evolves on the timescales of millions of years. Differences in ancestry and timing of the species' radiations can be related to the different biogeography of the two regions. This implies that the historical imprint on adaptive radiations could be predicted on the basis of the attributes of ancestors and biogeographical context.

Lovette, I. J., and E. Bermingham. 1999. Explosive speciation in the New World Dendroica warblers. Proceedings of the Royal Society of London: Biological Sciences 266, 1629-1636.

Abstract: The 27 species of Dendroica wood-warblers represent North America's most spectacular avian adaptive radiation. Dendroica species exhibit high levels of local sympatry and differ in plumage and song, but the group contrasts with other well-known avian adaptive radiations such as the Hawaiian Honeycreepers and Galapagos finches in that Dendroica species have differentiated modestly in morphometric traits related to foraging. Instead, sympatric Dendroica tend to partition resources behaviorally, and they have become a widely cited example of competitive exclusion. We explored the temporal structure of Dendroica diversification via a phylogeny based on 3639 nucleotides of protein-coding mitochondrial DNA. Taxa sampled included 60 individuals representing 24 Dendroica species and a variety of other paruline warbler and outgroup species. Mitochondrial divergences among Dendroica species were generally large (mean pairwise interspecific distances = 10.0%), and many species were rooted in a basal polytomy. The prevalence of long terminal branches indicates that these species have evolved efficient isolating mechanisms that have prevented mtDNA introgression despite the many opportunities for hybridization resulting from local sympatry. Comparisons with a null model of random bifurcation/extinction demonstrate that cladogenesis in Dendroica has been clustered nonrandomly with respect to time, with a significant burst of speciation occurring early in the history of the genus, possibly as long ago as the late Miocene or early Pliocene. Although this nonrandom clustering of speciation is consistent with the pattern expected of an adaptive radiation, the age of the Dendroica radiation suggests it is an "ancient species flock" in which most extant species represent lineages that have long been evolutionarily independent.

Lovette, I. J., E. Bermingham, S. Rohwer, and C. Wood. 1999. Mitochondrial RFLP and sequence variation among closely related avian species and the genetic characterization of hybrid Dendroica warblers. Molecular Ecology 8, 1431-1441.

Abstract: To address several interconnected goals, we used mitochondrial DNA (mtDNA) sequences to explore evolutionary relationships among four potentially hybridizing taxa in a North American avian superspecies (Dendroica occidentalis, D. townsendi, D. virens, and D. nigrescens). We first compared the results of a previous restriction fragment length polymorphism (RFLP)-based study with 1453 nucleotides from the mitochondrial cytochrome oxidase subunit I (COI), ATP-synthase 6 (ATPase 6), and ATP-synthase 8 (ATPase 8) genes. Separate phylogenetic analyses of the RFLP and sequence data provided identical and well-supported hierarchical species-level reconstructions that grouped occidentalis and townsendi as sister taxa. We then explored several general features of mitochondrial evolution via a comparison of the RFLP and sequence data sets. Qualitative rate differences that seemed evident in highly autocorrelated comparisons of RFLP vs. sequence pairwise distances were not supported when autocorrelation was removed. We also noted a high variance in corresponding RFLP and sequence distances after the removal of autocorrelation effects. This variance suggests that caution should be used when combining RFLP and sequence-based data in studies that require the large-scale synthesis of divergence estimates drawn from sources employing different molecular techniques. Finally, we used our parallel RFLP and sequence data to design and validate a rapid and inexpensive polymerase chain reaction-RFLP (PCR-RFLP) protocol for determining species-specific mitochondrial haplotypes. This PCR-RFLP technique will be applied in ongoing studies of the occidentalis/townsendi hybrid zone, where the historic and geographical complexity of the interbreeding populations necessitates the genotyping of thousands of individual warblers.

Lovette, I. J., E. Bermingham, and R. E. Ricklefs. 1999. Mitochondrial DNA phylogeography and the conservation of endangered Lesser Antillean Icterus Orioles. Conservation Biology, 13, 1088-1096.

Abstract: Recent natural and anthropogenic disturbances have endangered two of the three oriole species endemic to single islands in the Lesser Antilles. The ongoing eruption of the Soufriere Hills volcano may have doomed the Montserrat Oriole (Icterus oberi), whereas high levels of nest parasitism by a cowbird threaten the Martinique Oriole (I. bonana). These orioles and related Antillean and Central American forms have been considered part of the Icterus dominicensis superspecies complex, but the taxonomic status of the different Antillean island populations has been long debated. To investigate levels of evolutionary differentiation among threatened Lesser Antillean orioles, we analyzed 2507 nucleotides of protein-coding mitochondrial DNA (mtDNA) sequence from orioles on Martinique, Montserrat, St. Lucia (I. laudabilis), Puerto Rico (I. dominicensis dominicensis), Mexico (I. d. prosthemelas), and three Icterus outgroup species. Phylogenetic analyses of the mtDNA data supported the monophyly of Antillean members of the I. dominicensis complex and identified a star-like pattern of relationship among them. Mitochondrial distances between the Antillean populations were large (4.5-5.8% nucleotide divergence) and suggested that the Lesser Antillean orioles have been isolated evolutionarily from one another since the late Pliocene. The oriole taxa on Montserrat, Martinique, and St. Lucia meet species criteria under the phylogenetic species concept and represent evolutionarily significant units. The impending extinction of the phylogenetically unique Montserrat oriole highlights the vulnerability of island endemics to habitat degradation followed by rare and unpredictable natural catastrophes.

Lovette, I. J., G. Seutin, R. E. Ricklefs, and E. Bermingham. 1999. The assembly of an island fauna by natural invasion: Sources and temporal patterns in the avian colonization of Barbados. Biological Invasions 1, 33-41.

Abstract: By virtue of their isolation and depauperate faunas, oceanic islands offer unique opportunities to characterize the historical development of ecological communities derived from both natural and anthropogenic invasions. Barbados, an outlying island in the Lesser Antilles, was formed approximately 700,000 YBP by tectonic uplift and was then colonized by birds via natural invasion from the much older volcanic islands in the main Lesser Antillean arc. We investigated the timing and sources of the avian invasion of Barbados by determining levels of mitochondrial DNA (mtDNA) divergence between populations of eight bird species from Barbados and those on the nearby putative source islands of St. Lucia and St. Vincent. Although all Barbados populations appeared to be young relative to the geological age of the island, we found differences among species in their inferred times of colonization and we identified at least two sources of immigrants to Barbados. In contrast to these historical differences across species and populations, our characterization of the mitochondrial genotypes of 231 individual birds suggests that each island population represents the descendants of a single founding maternal lineage. Considered in concert, the results of this molecular survey indicate that the Barbados bird community is composed of species with different invasion histories, which in turn suggests that the island's community composition has changed repeatedly over its 700,000 year history.

Ricklefs, R. E. and I. J. Lovette. 1999. The roles of island area per se and habitat diversity in the species-area relationships of four Lesser Antillean faunal groups. Journal of Animal Ecology, 68, 1142-1160.

Abstract: 1. We analysed the relationships between species richness, island area, and habitat diversity for birds, bats, butterflies, and reptiles and amphibians on 19 islands in the Lesser Antilles. Habitat diversity was quantified by Simpson's index based on the total areas of five vegetation types on each island. Island area varied over two orders of magnitude (13-1510 km2) and habitat diversity varied between 1 and 3.7 equivalents of equally abundant habitat types. 2. Because the Lesser Antilles consist of an inner arc of high, volcanic islands and an outer arc of low-lying islands formed of uplifted marine sediments, correlations between area and elevation (r2 = 0.32) and between area and habitat diversity (r2 = 0.40) were weak. Habitat diversity was, however, strongly correlated with maximum island elevation (r2 = 0.85). 3. Simple correlations of species richness with island area were significant for all four faunal groups, and simple correlations of species richness with elevation and habitat were significant for all groups except bats. In multiple regressions of species richness on area and habitat diversity together, area was a significant effect for birds and bats, and habitat diversity was a significant effect for birds, butterflies, and reptiles and amphibians. 4. These results suggest that the four Lesser Antillean taxonomic groups differ in their responses to area and habitat diversity. For butterflies and for reptiles and amphibians, the relationship of species richness to area is probably a fortuitous consequence of a relationship between habitat diversity and area. Bird species richness responds independently to both habitat diversity and area, and bat species richness is influenced by area but not by habitat diversity. 5. We suggest that this variation is related to differences in several biological traits of the different faunal groups. Strong habitat-diversity effects are likely in taxa with high degrees of habitat specialization, populations large enough to have a low probability of stochastic extinction, life-cycles that include a resistant resting stage that reduces vulnerability to catastrophic extinction, or a combination of these traits. In contrast, strong area effects are likely in taxa with weak habitat specialization, low population density, or both. 6. At least in Lesser Antillean birds, it is unlikely that immigration depends on island size. Therefore, the species-area relationship for birds is probably generated by island-size-dependent extinction. Among the four taxonomic groups we studied, only butterflies are likely to show a 'rescue effect' stemming from frequent between-island movement of individuals, as only butterflies exhibited low levels of endemism and lacked a unique area effect for species richness. 7. Considered in concert, these taxon-specific differences demonstrate that both biological characteristics of organisms and geographical features of island groups mediate the relative contribution of island area and habitat diversity to variation in species richness.

Lovette, I. J., E. Bermingham, G. Seutin, and R. E. Ricklefs. 1998. Range disjunction and evolutionary differentiation in West Indian Dendroica warblers. Auk 115, 890-903.

Abstract: We explored the evolution of geographic distributions in archipelagos by comparing mitochondrial DNA (mtDNA) sequences and morphometric characters within and among conspecific populations of Adelaide's Warbler (Dendroica adelaidae), Plumbeous Warbler (D. plumbea), and Olive-capped Warbler (D. pityophila). Phylogenetic reconstructions were based upon 1,455 nucleotides of protein-coding mtDNA sequence from 53 individual warblers; morphological analyses employed three external measurements from a larger number of museum specimens. Of the three taxa studied, Adelaide's Warbler occupied the broadest and most fragmented geographical distribution and exhibited the greatest interpopulation differentiation in both mtDNA and morphology. Phylogenetic analyses demonstrated that the three Adelaide's Warbler populations are each reciprocally monophyletic with the Puerto Rican lineage basal to sister clades on Barbuda and St. Lucia. Genetic distances among these populations were comparable with those between some continental species. In contrast to the mtDNA pattern, the Puerto Rican and Barbudan Adelaide's Warbler populations were most similar in morphometry. We observed considerably less mtDNA and morphometric differentiation among populations of the two species with more restricted and less fragmented distributions, the Plumbeous Warbler of Dominica and Guadeloupe and the Olive-capped Warbler of the Bahamas and Cuba. High levels of molecular and morphological differentiation among the geographically disjunct Adelaide's Warbler populations and low differentiation in the two species with less fragmented ranges suggest that range disjunctions indicate the long-term evolutionary independence of geographically isolated island populations.

Lovette, I. J. and R. T. Holmes. 1995. Foraging behavior of American Redstarts in breeding and wintering habitats: Implications for relative food availability. Condor 97, 782-791.

Abstract: We investigated food availability for a long-distance migrant species, the American Redstart (Setophaga ruticilla), in both its summer breeding habitat in New Hampshire and in its winter habitat in Jamaica. We used four components of foraging behavior (prey attack rate, foraging speed, time spent foraging, and foraging maneuver use) as indicators of the relative availability of prey in the two seasons. Redstarts attacked prey at a significantly greater rate in summer than in winter, indicating that foraging birds encountered prey more frequently in summer. The winter prey-encounter rate was low even though redstarts moved almost twice as fast while foraging in winter as in summer. Male redstarts also spent more time foraging in winter (85%) than in summer (43-65%), possibly to balance the low rate at which they encountered prey. In winter, redstarts used more foraging maneuvers that were directed towards small flying prey, whereas in summer they used maneuvers that resulted in the capture of relatively large and presumably energy-rich prey such as lepidopteran larvae. That wintering redstarts foraged faster, attacked prey less often, and spent more time foraging than those in summer indicates that the winter is a period of relative food scarcity for this species, whereas the breeding season is a period of greater resource abundance.