Transoceanic Dispersal Events Research Articles

Out of the Neotropics: Late Cretaceous colonization of Australasia by American arthropods.

The origins of tropical southwest Pacific diversity are traditionally attributed to southeast Asia or Australia. Oceanic and fragment islands are typically colonized by lineages from adjacent continental margins, resulting in attrition of diversity with distance from the mainland. Here, we show that an exceptional tropical family of harvestmen with a trans-Pacific disjunct distribution has its origin in the Neotropics. We found in a multi-locus phylogenetic analysis that the opilionid family Zalmoxidae, which is distributed in tropical forests on both sides of the Pacific, is a monophyletic entity with basal lineages endemic to Amazonia and Mesoamerica. Indo-Pacific Zalmoxidae constitute a nested clade, indicating a single colonization event. Lineages endemic to putative source regions, including Australia and New Guinea, constitute derived groups. Divergence time estimates and probabilistic ancestral area reconstructions support a Neotropical origin of the group, and a Late Cretaceous (ca 82 Ma) colonization of Australasia out of the Fiji Islands and/or Borneo, which are consistent with a transoceanic dispersal event. Our results suggest that the endemic diversity within traditionally defined zoogeographic boundaries might have more complex evolutionary origins than previously envisioned.

Biogeographical origins and diversification of the exoneurine allodapine bees of Australia (Hymenoptera, Apidae)

Aim Early diversification of allodapine bees occurred in Africa c. 50 Ma. They are most abundant in sub-Saharan Africa and Australia, and one of the oldest phylogenetic divergences in the tribe involves a split between an African + Malagasy clade and an Australian clade. The historical biogeographical scenario for this has been highly problematic, entailing an Eocene dispersal from Africa to Australia, followed by an unresolved, and apparently rapid, set of bifurcations leading to the Australian ‘exoneurine’ genera. Here we use an expanded taxon set of Australian species to explore the timing and historical biogeography of the exoneurine radiation. Location Australia, Africa, Madagascar. Methods One nuclear gene (F2 copy of elongation factor 1α) and two mitochondrial genes (cytochrome c oxidase subunit I and cytochrome b) were sequenced for 33 Australian exoneurine species from all five genera found on the continent, as well as for an additional 37 species from all non-parasitic genera in the remainder of the tribe. We used Bayesian inference analyses to study phylogenetic topology and penalized likelihood analyses to infer key dates of divergence within the tribe. We also used lineage-through-time (LTT) analyses and Bayesian analyses to explore the tempo of radiations and biogeographical history of the exoneurines. Results Results from the phylogenetic analyses were congruent with previous studies, indicating a single colonization event c. 34 Ma, too late for Gondwanan vicariance models, and too early for a Laurasian dispersal route. In contrast to earlier studies, we show that this colonization event did not result in an ancient rapid radiation. However, LTT patterns indicated a rapid radiation of the temperate-adapted genera Exoneura and Brevineura, but not of the xeric-adapted genus Exoneurella, from 10 to 6 Ma. Main conclusions Our results indicate a trans-oceanic dispersal event from Africa to Australia, most likely via Antarctica, with an accelerated diversification of temperate-adapted lineages during the major Late Miocene event referred to as the ‘Hill Gap’. This is the first study to link radiations in Australian bee faunal elements to changing climate, and differs from many other plant and insect phylogenetic studies by showing increased radiation of temperate clades, rather than xeric clades, with increasing aridification of Australia.

Systematics and biogeography of the Gondwanan Orthocladiinae (Diptera: Chironomidae)

Restrictions to effective dispersal and gene flow caused by the fragmentation of ancient supercontinents are considered to have driven diversification and speciation on disjunct landmasses globally. Investigating the role that these processes have played in the development of diversity within and among taxa is crucial to understanding the origins and evolution of regional biotas. Within the chironomid (non-biting midge) subfamily Orthocladiinae (Diptera: Chironomidae), a group of genera that are distributed across the austral continents (Australia, New Zealand, South America) have been proposed to represent a relict Gondwanan clade. We used a molecular approach to resolve relationships among taxa with the aim to determine the relative roles that vicariance and dispersal may have played in the evolution of this group. Continental biotas did not form monophyletic groups, in accordance with expectations given existing morphological evidence. Patterns of phylogenetic relationships among taxa did not accord with expected patterns based on the geological sequence of break-up of the Gondwanan supercontinent. Likewise, divergence time estimates, particularly for New Zealand taxa, largely post-dated continental fragmentation and implied instead that several transoceanic dispersal events may have occurred post-vicariance. Passive dispersal of gravid female chironomid adults is the most likely mechanism for transoceanic movement, potentially facilitated by West Wind Drift or anti-cyclone fronts. Estimated timings of divergence among Australian and South American Botryocladius, on the other hand, were congruent with the proposed ages of separation of the two continents from Antarctica. Taken together, these data suggest that a complex relationship between both vicariance and dispersal may explain the evolution of this group. The sampling regime we implemented here was the most intensive yet performed for austral members of the Orthocladiinae and unsurprisingly revealed several novel taxa that will require formal description.

The evolution of Cayaponia (Cucurbitaceae): Repeated shifts from bat to bee pollination and long‐distance dispersal to Africa 2–5 million years ago

The Cucurbitaceae genus Cayaponia comprises ∼60 species that occur from Uruguay to the southern United States and the Caribbean; C. africana occurs in West Africa and on Madagascar. Pollination is by bees or bats, raising the question of the evolutionary direction and frequency of pollinator shifts. Studies that investigated such shifts in other clades have suggested that bat pollination might be an evolutionary end point. • Plastid and nuclear DNA sequences were obtained for 50 accessions representing 30 species of Cayaponia and close relatives, and analyses were carried out to test monophyly, infer divergence times, and reconstruct ancestral states for habitat preferences and pollination modes. • The phylogeny shows that Cayaponia is monophyletic as long as Selysia (a genus with four species from Central and South America) is included. The required nomenclatural transfers are made in this paper. African and Madagascan accessions of C. africana form a clade that is part of a polytomy with Caribbean and South American species, and the inferred divergence time of 2-5 Ma implies a transoceanic dispersal event from the New World to Africa. The ancestral state reconstructions suggest that Cayaponia originated in tropical forests from where open savannas were reached several times and that bee pollination arose from bat pollination, roughly concomitant with the shifts from forests to savanna habitats. • Cayaponia provides the first example of evolutionary transitions from bat to bee pollination as well as another instance of transoceanic dispersal from the New World to Africa.

Evolution and biogeography of primates: a new model based on molecular phylogenetics, vicariance and plate tectonics

Heads, M. Evolution and biogeography of primates: a new model based on molecular phylogenetics, vicariance and plate tectonics. —Zoologica Scripta, 39, 107–127. The ages of the oldest fossils suggest an origin for primates in the Paleocene (∼56 Ma). Fossil-calibrated molecular clock dates give Cretaceous dates (∼80–116 Ma). Both these estimates are minimum dates although they are often ‘transmogrified’ and treated as maximum or absolute dates. Oldest fossils can underestimate ages by tens of millions of years and instead of calibrating the time-course of evolution with a scanty fossil record, the geographical boundaries of the main molecular clades of primates are calibrated here with radiometrically dated tectonic events. This indicates that primates originated when a globally widespread ancestor (early Archonta) differentiated into a northern group (Plesiadapiformes, extinct), a southern group (Primates), and two south-east Asian groups (Dermoptera and Scandentia). The division occurred with the breakup of Pangea in the Early Jurassic and the opening of the central Atlantic (∼185 Ma). Within primates, the strepsirrhines and haplorhines diverged with volcanism and buckling on the Lebombo Monocline, a volcanic rifted margin in south-east Africa (Early Jurassic, ∼180 Ma). Within strepsirrhines, lorises and galagos (Africa and Asia) and lemurs (Madagascar) diverged with the formation of the Mozambique Channel (Middle Jurassic, ∼160 Ma). Within haplorhines, Old World monkeys and New World monkeys diverged with the opening of the Atlantic (Early Cretaceous, ∼130 Ma). The main aspects of primate distribution are interpreted as the result of plate tectonics, phylogeny and vicariance, with some subsequent range expansion leading to secondary overlap. Long-distance, trans-oceanic dispersal events are not necessary. The primate ancestral complex was already widespread globally when sea-floor spreading, strike-slip rifting and orogeny fractured and deformed distributions through the Jurassic and Cretaceous, leading to the origin of the modern clades. The model suggests that the topology of the phylogenetic tree reflects a sequence of differentiation in a widespread ancestor rather than a series of dispersal events.

The evolutionary diversification of parrots supports a taxon pulse model with multiple trans-oceanic dispersal events and local radiations

Vicariance is thought to have played a major role in the evolution of modern parrots. However, as the relationships especially of the African taxa remained mostly unresolved, it has been difficult to draw firm conclusions about the roles of dispersal and vicariance. Our analyses using the broadest taxon sampling of old world parrots ever based on 3219bp of three nuclear genes revealed well-resolved and congruent phylogenetic hypotheses. Agapornis of Africa and Madagascar was found to be the sister group to Loriculus of Australasia and Indo-Malayasia and together they clustered with the Australasian Loriinae, Cyclopsittacini and Melopsittacus. Poicephalus and Psittacus from mainland Africa formed the sister group of the Neotropical Arini and Coracopsis from Madagascar and adjacent islands may be the closest relative of Psittrichas from New Guinea. These biogeographic relationships are best explained by independent colonization of the African continent via trans-oceanic dispersal from Australasia and Antarctica in the Paleogene following what may have been vicariance events in the late Cretaceous and/or early Paleogene. Our data support a taxon pulse model for the diversification of parrots whereby trans-oceanic dispersal played a more important role than previously thought and was the prerequisite for range expansion into new continents.

Speciation of a tropical fungal species pair following transoceanic dispersal

This study focuses on a pair of fungal species, Moelleriella libera and M. raciborskii (Ascomycota: Clavicipitaceae) from the neotropics and paleotropics, respectively, that are phenotypically nearly indistinguishable. Molecular analyses based on DNA sequences from RNA polymerase II subunit 2 (RPB2), translation elongation factor 1-α (EF1-α) and β-tubulin genes confirm that they are recently derived sister species. Speciation appears to have followed an historical transoceanic dispersal event. Models of population structure and migration from TCS, IM, and coalescent-based analyses suggest there is little gene flow between the two species. The direction of dispersal, investigated using the progression rule and coalescent-based gene genealogies, was likely from the New World to the Old World.

The age and biogeography of Citrus and the orange subfamily (Rutaceae: Aurantioideae) in Australasia and New Caledonia

The geological history of Australasia, New Caledonia, and Southeast Asia, has been complex, resulting in competing biogeographic hypotheses for taxa found here. Alternative hypotheses-Gondwanan vicariance, rafting terranes, long-distance dispersal-may be distinguished by different predicted divergence times between disjunct sister taxa. Taxa within Rutaceae subfamily Aurantioideae are ideal for testing these hypotheses because of their distributions. Therefore, the ages of Rutaceae and Aurantioideae were estimated using molecular dating. One data set comprised 51 sequences of rbcL and atpB with sampling across rosids and three fossil calibrations: crown Fabales+Fagales+Rosales (>94 Ma), Fabaceae (>51 Ma) and stem Ailanthus, Simaroubaceae (>52 Ma). Another data set comprised 81 Aurantioideae using >8 kb of chloroplast sequence and secondary calibration. Confidence in estimated divergence times was explored by varying the root age, dating method (strict, local, and relaxed clocks), and inclusion of internal calibrations. We conclude that the Rutaceae crown diverged in the Eocene (36.4-56.8 Ma, mean 47.6), whereas the Aurantioideae crown originated in the early Miocene (12.1-28.2 Ma, mean 19.8). This young age suggests that Gondwanan vicariance does not explain the distributions of extant Aurantioideae. Taxa found in New Caledonia may have arrived by separate transoceanic dispersal events.

Phylogenetic relationships within Dendroligotrichum and Polytrichadelphus (Polytrichaceae, Polytrichopsida) in the Palaeoaustral region. Studies in austral temperate rainforest bryophytes 32

Plastid trnT–F and atpB–rbcL spacer sequences as well as AFLP fingerprints are utilised to infer phylogenetic relationships of Dendroligotrichum and Polytrichadelphus taxa (Polytrichaceae) in the palaeoaustral region. Phylogenies based on DNA sequence data support the monophyly of each genus. Relationships within Dendroligotrichum remain ambiguous owing to low sequence divergence. AFLP fingerprinting, however, allows a clear distinction of all included Dendroligotrichum and Polytrichadelphus taxa at the species level. The morphological, distributional, ecological and molecular differences justify the recognition of the following three species in Dendroligotrichum: D. dendroides (Brid. ex Hedw.) Broth. and D. squamosum (Hook.f. & Wilson) Cardot in southern South America, as well as D. microdendron (Müll. Hal.) G.L.Sm. in New Zealand; and the following two species in Polytrichadelphus: P. magellanicus (Hedw.) Mitt. s.str. in southern South America and P. innovans (Müll. Hal.) A.Jäger in Australia and New Zealand. For Polytrichadelphus, the molecular topologies correspond with a vicariance scenario, with a basic split of taxa in the palaeoaustral region followed by migration of southern South American taxa northwards into the Neotropics. In Dendroligotrichum, substitutions and indels in the trnL intron and atpB–rbcL spacer are ambiguous in supporting either a basic split between the South American species and D. microdendron, similar to the one in Polytrichadelphus, or a trans-oceanic dispersal event between New Zealand and southern South America.

Tropical Intercontinental Disjunctions: Gondwana Breakup, Immigration from the Boreotropics, and Transoceanic Dispersal

With the advent of molecular data, and particularly the use of molecular clocks when warranted, biogeographers have begun to reexamine the roles of Gondwana breakup, immigration from the Laurasian tropics, and transoceanic dispersal in shaping similarities among the world’s tropical floras (Givnish et al. 1999, 2000; Lavin et al. 2000, 2005; Renner et al. 2000, 2001; Azuma et al. 2001; Chanderbali et al. 2001; Renner and Meyer 2001; Conti et al. 2002; Davis et al. 2002; Jobson et al. 2003; Zhang and Renner 2003; Berry et al. 2004). As increasing numbers of continental disjunctions are analyzed, it has also become possible to ask whether there are regular patterns in the directions and timing of transoceanic dispersal events (S. S. Renner, in this issue). Wind and ocean surface currents (as well as tectonics) all affect dispersal and are not randomly distributed in space and time; they should thus leave an evolutionary trace provided that they have been stable long enough to override lineage-specific differences in dispersal and establishment capability (e.g., see Munoz et al. 2004). Tropical intercontinental disjunctions raise issues analogous to those involving disjunct temperate floras in the Northern Hemisphere (see IJPS symposium edited by Manos and Donoghue [2001]), but the ocean gulfs are often greater and the latitudinal distributions of taxa less dynamic. Similar issues also emerge in studying the origin of island lineages (Wagner and Funk 1995; Givnish 1998; Emerson 2002). Insular groups pose special problems, especially when extraordinary divergence due to adaptive radiation makes it difficult to identify mainland ancestors or relatives. Yet intercontinental disjunctions can be even more complex to decipher, given the frequent lack of asymmetries between potential source and target areas (but see T. J. Givnish et al.; K. J. Sytsma et al.), the existence of direct connections to other landmasses at various times, and the longer and more complex tectonic histories of the terrains. The papers collected here represent the product of a symposium held in Madison during August 2002, sponsored by the Association for Tropical Biology and the Association for Systematic Botany and honoring Robert Thorne for his outstanding contributions to biogeography and especially to the analysis of tropical plant disjunctions (Thorne 1972, 1973; R. Thorne’s ‘‘reflections’’ at the end of this volume provide an entry into his biogeographic contributions). We invited researchers to present analyses based on molecular data for a variety of disjunctly distributed tropical lineages that, in aggregate, display a diversity of continental disjunctions, mechanisms of dispersal, and geological age. We asked each contributor to address three questions: (1) How much information about the timing and nature of the events causing disjunctions can be obtained from molecular data? (2) What appear to be the relative roles of dispersal and vicariance, and how do these relate to events in Earth history? and (3) How can we cross-check and validate our inferences using fossils or other data? All of the contributions calibrate the lengths of branches in molecular trees (measured as the numbers of inferred nucleotide substitutions) against the apparent age of one or more ancestral taxa (inferred from the geological age of the oldest known fossil attributed to those taxa). The absolute dates of cladogenetic events within a lineage are then inferred using one or more of several calibration models and attributed to apparent dispersal or vicariance events, which have themselves been inferred from the distributions of modern-day taxa and their phylogenetic relationships to each other. The timing of range expansions is finally tied to shifts in geography, climate, or likely pathways for dispersal during geological time, and conclusions are drawn about the likely mechanisms underlying a particular disjunct distribution. The validity of such conclusions thus hinges on the completeness of our knowledge of the fossil record, both in areal extent and in time; on uncertainties in the branch lengths inferred from particular molecular markers; on the validity of chronological calibrations based on particular models and a particular set of fossil dates; and on uncertainties regarding the distributions of ancestral taxa inferred from a molecular phylogeny, distributions of modern-day taxa, and particular models for shifts in geographic range. Nevertheless, the approaches taken by papers in this symposium, involving the complementary use of molecular and paleobotanical data, offer some of the most powerful techniques now available for assessing the age—and, hence, the mechanism—associated with a shift in the range of a lineage. Without such approaches, or comprehensive and thus perhaps unattainable fossil data bearing on the timing of a range shift, one might indiscriminately invoke long-distance dispersal, continental drift, or boreotropical migration to explain essentially any tropical disjunction. The surprising conclusion from careful analyses in this symposium and elsewhere (e.g., Cronn and Wendel 2004; Lavin et al. 2005) is that long-distance dispersal may be more pervasive than all but its most ardent advocates (e.g., Iltis 1967) had previously proposed.