Ben H. Warren

Global phylogeographic limits of Hawaii's avian malaria

The introduction of avian malaria (Plasmodium relictum) to Hawaii has provided a model system for studying the influence of exotic disease on naive host populations. Little is known, however, about the origin or the genetic variation of Hawaiis malaria and traditional classification methods have confounded attempts to place the parasite within a global ecological and evolutionary context. Using fragments of the parasite mitochondrial gene cytochrome b and the nuclear gene dihydrofolate reductase-thymidylate synthase obtained from a global survey of greater than 13 000 avian samples, we show that Hawaiis avian malaria, which can cause high mortality and is a major limiting factor for many species of native passerines, represents just one of the numerous lineages composing the morphological parasite species. The single parasite lineage detected in Hawaii exhibits a broad host distribution worldwide and is dominant on several other remote oceanic islands, including Bermuda and Moorea, French Polynesia. The rarity of this lineage in the continental New World and the restriction of closely related lineages to the Old World suggest limitations to the transmission of reproductively isolated parasite groups within the morphological species.

Why does the biota of the Madagascar region have such a strong Asiatic flavour

A corollary of island biogeographical theory is that islands are largely colonized from their nearest mainland source. Despite Madagascar’s extreme isolation from India and proximity to Africa, a high proportion of the biota of the Madagascar region has Asian affinities. This pattern has rarely been viewed as surprising, as it is consistent with Gondwanan vicariance. Molecular phylogenetic data provide strong support for such Asian affinities, but often not for their vicariant origin; most divergences between lineages in Asia and the Madagascar region post‐date the separation of India and Madagascar considerably (up to 87 Myr), implying a high frequency of dispersal that mirrors colonization of the Hawaiian archipelago in distance. Indian Ocean bathymetry and the magnitude of recent sea‐level lowstands support the repeated existence of sizeable islands across the western Indian Ocean, greatly reducing the isolation of Madagascar from Asia. We put forward predictions to test the role of this historical factor in the assembly of the regional biota.

Molecular Phylogeography Reveals Island Colonization History and Diversification of Western Indian Ocean Sunbirds (Nectarinia: Nectariniidae)

We constructed a phylogenetic hypothesis for western Indian Ocean sunbirds (Nectarinia) and used this to investigate the geographic pattern of their diversification among the islands of the Indian Ocean. A total of 1309 bp of mitochondrial sequence data was collected from the island sunbird taxa of the western Indian Ocean region, combined with sequence data from a selection of continental (African and Asian) sunbirds. Topological and branch length information combined with estimated divergence times are used to present hypotheses for the direction and sequence of colonization events in relation to the geological history of the Indian Ocean region. Indian Ocean sunbirds fall into two well-supported clades, consistent with two independent colonizations from Africa within the last 3.9 million years. The first clade contains island populations representing the species Nectarinia notata, while the second includes Nectarinia souimanga, Nectarinia humbloti, Nectarinia dussumieri, and Nectarinia coquereli. With respect to the latter clade, application of Bremers [Syst. Biol. 41 (1992) 436] ancestral areas method permits us to posit the Comoros archipelago as the point of initial colonization in the Indian Ocean. The subsequent expansion of the souimanga clade across its Indian Ocean range occurred rapidly, with descendants of this early expansion remaining on the Comoros and granitic Seychelles. The data suggest that a more recent expansion from Anjouan in the Comoros group led to the colonization of Madagascar by sunbirds representing the souimanga clade. In concordance with the very young geological age of the Aldabra group, the sunbirds of this archipelago have diverged little from the Madagascar population; this is attributed to colonization of the Aldabra archipelago in recent times, in one or possibly two or more waves originating from Madagascar. The overall pattern of sunbird radiation across Indian Ocean islands indicates that these birds disperse across ocean barriers with relative ease, but that their subsequent evolutionary success probably depends on a variety of factors including prior island occupation by competing species.

Immigration, species radiation and extinction in a highly diverse songbird lineage: white-eyes on Indian Ocean islands

Molecular phylogenetic hypotheses of species‐rich lineages in regions where geological history can be reliably inferred may provide insights into the scale of processes driving diversification. Here we sample all extant or recently extinct white‐eye (Zosterops) taxa of the southwest Indian Ocean, combined with samples from all principal continental lineages. Results support a high dispersal capability, with at least two independent continental sources for white‐eyes of the region. An early (within 1.8 million years ago) expansion into the Indian Ocean may have originated either from Asia or Africa; the three resulting lineages show a disparate distribution consistent with considerable extinction following their arrival. Africa is supported as the origin of a later expansion into the region (within 1.2 million years ago). On two islands, a pair of Zosterops species derived from independent immigrations into the Indian Ocean co‐occur or may have formerly co‐occurred, providing strong support for their origin by double‐island colonization rather than within‐island (sympatric or microallopatric) speciation. On Mauritius and La Réunion, phylogenetic placement of sympatric white‐eyes allow us to rule out a scenario in which independent within‐island speciation occurred on both islands; one of the species pairs must have arisen by double colonization, while the other pair is likely to have arisen by the same mechanism. Long‐distance immigration therefore appears to be responsible for much of the regions white‐eye diversity. Independent immigrations into the region have resulted in lineages with mutually exclusive distributions and it seems likely that competition with congeneric species, rather than arrival frequency, may limit present‐day diversity.

The geographic scale of diversification on islands: genetic and morphological divergence at a very small spatial scale in the Mascarene grey white-eye (Aves: Zosterops borbonicus)

BackgroundOceanic islands provide unique scenarios for studying the roles of geography and ecology in driving population divergence and speciation. Assessing the relative importance of selective and neutral factors in driving population divergence is central to understanding how such divergence may lead to speciation in small oceanic islands, where opportunities for gene flow and population mixing are potentially high. Here we report a case of genetic and morphological structure in the Mascarene grey white-eye (Zosterops borbonicus) a species that shows a striking, geographically structured plumage polymorphism on the topographically and ecologically complex island of Réunion, yet is monotypic on the relatively uniform neighbouring island of Mauritius.ResultsAnalysis of 276 AFLP loci in 197 individuals revealed prolonged independent evolution of Réunion and Mauritius populations, which is congruent with previous mtDNA assessments. Furthermore, populations on Réunion showed significant differentiation into three main genetic groups separating lowland from highland areas despite the small geographic distances involved. Genetic differentiation along the altitudinal gradient is consistent with morphometric analysis of fitness-related traits. Birds in the highlands were larger, yet had relatively smaller beaks than in the lowlands, suggesting the role of selection in shaping morphology and restricting gene flow along the gradient. No genetic differentiation between plumage morphs was detected in neutral markers, suggesting that plumage differences are of recent origin.ConclusionsOur results suggest a dual role of vicariance and natural selection in differentiating populations of a passerine bird in an oceanic island at very small spatial scales. We propose a combination of past microallopatry driven by volcanic activity and selection-constrained dispersal along steep ecological gradients to explain the striking levels of population structure found within the island, although the possibility that genetic differences evolved in situ along the gradient cannot be ruled out at present. The lack of congruence between genetic groups and plumage morphs suggests that the latter are of recent origin and likely due to social or sexual selection acting on few loci. The presence of sharp and stable contact zones between plumage morphs suggests that they could be on independent evolutionary trajectories, yet whether or not they represent incipient species will require further research to directly assess the degree of reproductive isolation among them.

Rapid parallel evolution of aberrant traits in the diversification of the Gulf of Guinea white-eyes (Aves, Zosteropidae).

Archipelago‐endemic bird radiations are familiar to evolutionary biologists as key illustrations of evolutionary patterns. However, such radiations are in fact rare events. White‐eyes (Zosteropidae) are birds with an exceptionally high colonization and speciation potential; they have colonized more islands globally than any other passerine group and include the most species‐rich bird genus. The multiplication of white‐eye island endemics has been consistently attributed to independent colonizations from the mainland; the white‐eyes of the Gulf of Guinea archipelago had been seen as a classic case, spanning as great a breadth of phenotypic diversity as the family worldwide. Contrary to this hypothesis, our molecular phylogenetic analysis places the Gulf of Guinea white‐eyes in just two radiations, one grouping all five oceanic island taxa and the other grouping continental island and land‐bridge taxa. Numerous ‘aberrant’ phenotypes (traditionally grouped in the genus Speirops) have evolved independently over a short space of time from nonaberrant (Zosterops) phenotypes; the most phenotypically divergent species have separated as recently as 0.22 Ma. These radiations rival those of Darwin’s finches and the Hawaiian honeycreepers in terms of the extent of adaptive radiation per unit time, both in terms of species numbers and in terms of phenotypic diversity. Tempo and patterns of morphological divergence are strongly supportive of an adaptive radiation in the oceanic islands driven by ecological interactions between sympatric white‐eyes. Here, very rapid phenotypic evolution mainly affected taxa derived from the youngest wave of colonization, in accordance with the model of asymmetric divergence owing to resource competition in sympatry.

HYBRIDIZATION AND BARRIERS TO GENE FLOW IN AN ISLAND BIRD RADIATION

While reinforcement may play a role in all major modes of speciation, relatively little is known about the timescale over which species hybridize without evolving complete reproductive isolation. Birds have high potential for hybridization, and islands provide simple settings for uncovering speciation and hybridization patterns. Here we develop a phylogenetic hypothesis for a phenotypically diverse radiation of finch‐like weaver‐birds (Foudia) endemic to the western Indian Ocean islands. We find that unlike Darwins finches, each island‐endemic Foudia population is a monophyletic entity for which speciation can be considered complete. In explaining the only exceptions—mismatches between taxonomy, mitochondrial, and nuclear data—phylogenetic and coalescent methods support introgressive hybridization rather than incomplete lineage sorting. Human introductions of known timing of one island‐endemic species, to all surrounding archipelagos provide two fortuitous experiments; (1) population sampling at known times in recent evolutionary history, (2) bringing allopatric lineages of an island radiation into secondary contact. Our results put a minimum time bound on introgression (235 years), and support hybridization between species in natural close contact (parapatry), but not between those in natural allopatry brought into contact by human introduction. Time in allopatry, rather than in sympatry, appears key in the reproductive isolation of Foudia species.

Molecular characterization of trophic ecology within an island radiation of insect herbivores (Curculionidae: Entiminae: Cratopus)

The phytophagous beetle family Curculionidae is the most species‐rich insect family known, with much of this diversity having been attributed to both co‐evolution with food plants and host shifts at key points within the early evolutionary history of the group. Less well understood is the extent to which patterns of host use vary within or among related species, largely because of the technical difficulties associated with quantifying this. Here we develop a recently characterized molecular approach to quantify diet within and between two closely related species of weevil occurring primarily within dry forests on the island of Mauritius. Our aim is to quantify dietary variation across populations and assess adaptive and nonadaptive explanations for this and to characterize the nature of a trophic shift within an ecologically distinct population within one of the species. We find that our study species are polyphagous, consuming a much wider range of plants than would be suggested by the literature. Our data suggest that local diet variation is largely explained by food availability, and locally specialist populations consume food plants that are not phylogenetically novel, but do appear to represent a novel preference. Our results demonstrate the power of molecular methods to unambiguously quantify dietary variation across populations of insect herbivores, providing a valuable approach to understanding trophic interactions within and among local plant and insect herbivore communities.

The distribution of species diversity across a flora's component lineages: dating the Cape's ‘relicts’

The Cape Floristic Region is exceptionally species-rich both for its area and latitude, and this diversity is highly unevenly distributed among genera. The modern flora is hypothesized to result largely from recent (post-Oligocene) speciation, and it has long been speculated that particular species-poor lineages pre-date this burst of speciation. Here, we employ molecular phylogenetic data in combination with fossil calibrations to estimate the minimum duration of Cape occupation by 14 unrelated putative relicts. Estimates vary widely between lineages (7–101 Myr ago), and when compared with the estimated timing of onset of the modern floras radiation, it is clear that many, but possibly not all, of these lineages pre-date its establishment. Statistical comparisons of diversities with lineage age show that low species diversity of many of the putative relicts results from a lower rate of diversification than in dated Cape radiations. In other putative relicts, however, we cannot reject the possibility that they diversify at the same underlying rate as the radiations, but have been present in the Cape for insufficient time to accumulate higher diversity. Although the extremes in diversity of currently dated Cape lineages fall outside expectations under a constant underlying diversification rate, sampling of all Cape lineages would be required to reject this null hypothesis.

Diversity and distribution of avian haematozoan parasites in the western Indian Ocean region: a molecular survey

The genetic diversity of haematozoan parasites in island avifauna has only recently begun to be explored, despite the potential insight that these data can provide into the history of association between hosts and parasites and the possible threat posed to island endemics. We used mitochondrial DNA sequencing to characterize the diversity of 2 genera of vector-mediated parasites (Plasmodium and Haemoproteus) in avian blood samples from the western Indian Ocean region and explored their relationship with parasites from continental Africa. We detected infections in 68 out of 150 (45·3%) individuals and cytochrome b sequences identified 9 genetically distinct lineages of Plasmodium spp. and 7 lineages of Haemoproteus spp. We found considerable heterogeneity in parasite lineage composition across islands, although limited sampling may, in part, be responsible for perceived differences. Two lineages of Plasmodium spp. and 2 lineages of Haemoproteus spp. were shared by hosts in the Indian Ocean and also on mainland Africa, suggesting that these lineages may have arrived relatively recently. Polyphyly of island parasites indicated that these parasites were unlikely to constitute an endemic radiation and instead probably represent multiple colonization events. This study represents the first molecular survey of vector-mediated parasites in the western Indian Ocean, and has uncovered a diversity of parasites. Full understanding of parasite community composition and possible threats to endemic avian hosts will require comprehensive surveys across the avifauna of this region.