Land Bridges and Rafting Theories to Explain Terrestrial-Vertebrate Biodiversity on Madagascar.

Madagascar's celebrated land-vertebrate assemblage has long been studied and discussed. How the ancestors of the 30 different lineages arrived on the island, which has existed since 85 Mya and is separated from neighboring Africa by 430 km of water, is a deeply important question. Did the colonizations take place when the landmass formed part of Gondwana, or did they occur later and involve either now-drowned causeways or overwater dispersal (on vegetation rafts or by floating/swimming)? Following a historical review, we appraise the geological-geophysical evidence and the faunal-suite colonization record. Twenty-six of the clades are explained by temporally stochastic overwater dispersals, spanning 69-0 Mya, while two others are considered Gondwanan vicariant relicts. Due to a lack of information, the remaining two groups cannot be evaluated. The findings thus appear to resolve a debate that has rumbled along, with sporadic eruptions, since the mid-1800s.

The colonisation of Madagascar by land-bound vertebrates.

Despite discussions extending back almost 160 years, the means by which Madagascar's iconic land vertebrates arrived on the island remains the focus of active debate. Three options have been considered: vicariance, range expansion across land bridges, and dispersal over water. The first assumes that a group (clade/lineage) occupied the island when it was connected with the other Gondwana landmasses in the Mesozoic. Causeways to Africa do not exist today, but have been proposed by some researchers for various times in the Cenozoic. Over-water dispersal could be from rafting on floating vegetation (flotsam) or by swimming/drifting. A recent appraisal of the geological data supported the idea of vicariance, but found nothing to justify the notion of past causeways. Here we review the biological evidence for the mechanisms that explain the origins of 28 of Madagascar's land vertebrate clades [two other lineages (the geckos Geckolepis and Paragehyra) could not be included in the analysis due to phylogenetic uncertainties]. The podocnemid turtles and typhlopoid snakes are conspicuous for they appear to have arisen through a deep-time vicariance event. The two options for the remaining 26 (16 reptile, five land-bound-mammal, and five amphibian), which arrived between the latest Cretaceous and the present, are dispersal across land bridges or over water. As these would produce very different temporal influx patterns, we assembled and analysed published arrival times for each of the groups. For all, a 'colonisation interval' was generated that was bracketed by its 'stem-old' and 'crown-young' tree-node ages; in two instances, the ranges were refined using palaeontological data. The synthesis of these intervals for all clades, which we term a colonisation profile, has a distinctive shape that can be compared, statistically, to various models, including those that assume the arrivals were focused in time. The analysis leads us to reject the various land bridge models (which would show temporal concentrations) and instead supports the idea of dispersal over water (temporally random). Therefore, the biological evidence is now in agreement with the geological evidence, as well as the filtered taxonomic composition of the fauna, in supporting over-water dispersal as the mechanism that explains all but two of Madagascar's land-vertebrate groups.

Ancient DNA elucidates the lost world of western Indian Ocean giant tortoises and reveals a new extinct species from Madagascar.

Before humans arrived, giant tortoises occurred on many western Indian Ocean islands. We combined ancient DNA, phylogenetic, ancestral range, and molecular clock analyses with radiocarbon and paleogeographic evidence to decipher their diversity and biogeography. Using a mitogenomic time tree, we propose that the ancestor of the extinct Mascarene tortoises spread from Africa in the Eocene to now-sunken islands northeast of Madagascar. From these islands, the Mascarenes were repeatedly colonized. Another out-of-Africa dispersal (latest Eocene/Oligocene) produced on Madagascar giant, large, and small tortoise species. Two giant and one large species disappeared c. 1000 to 600 years ago, the latter described here as new to science using nuclear and mitochondrial DNA. From Madagascar, the Granitic Seychelles were colonized (Early Pliocene) and from there, repeatedly Aldabra (Late Pleistocene). The Granitic Seychelles populations were eradicated and later reintroduced from Aldabra. Our results underline that integrating ancient DNA data into a multi-evidence framework substantially enhances the knowledge of the past diversity of island faunas.

Wallace's line, Wallacea, and associated divides and areas: history of a tortuous tangle of ideas and labels.

Due to its position between the highly distinct Oriental and Australasian biogeographical realms, much effort has been spent demarcating associated separations and transitions in the faunal assemblages of the Indo-Australian Archipelago. Initially, sharp boundary lines were proposed, with the earliest dating from the mid-1800s. Notably, the one published by Alfred R. Wallace in 1863, based upon land-mammal and land-bird distributions, has since achieved iconic status and today its significance is recognized well beyond the confines of the biogeography community. Over the next four decades many such divides were engraved onto plates and inked onto charts of SE Asia using additional information, different organisms or other criteria. However, it became apparent that, as Wallace had noted, all such lines were to some degree permeable, and by the 1880s transition zones were being put forward instead; the label 'Wallacea' was introduced in 1924. Interestingly, the last decade has seen new divides and sub-regions being proposed, some departing markedly from earlier offerings. Although currently there is general agreement regarding much of the terminology associated with both the lines and the areas, the record of publication indicates that this consensus has emerged obliquely, and in some cases is weakly founded. This review does not present new data nor new analyses; rather it summarizes the development of ideas and reflects upon attendant issues that have emerged. After reviewing the key proposals, recommendations are presented that should in future alleviate perceived difficulties or inadequacies. Reference to specific divides must be true to their original definitions; there are many instances where the secondary literature has portrayed them incorrectly and with some this has rippled through into later publications. Moreover, Wallace's 1863 line is not the one that he finally settled upon (in 1910); its path around Sulawesi was transferred from the west to the east of the Island. Ideally, Huxley's divide (1868) should carry his name rather than Wallace's; the latter never accepted the proposition. Lydekker's Line (1896) ought to be labelled the Heilprin-Lydekker Line in recognition of Angelo Heilprin's 1887 contribution. Concerning transition zones, ideally Wallacea should correspond to its original 1924 description, which incorporated the Philippine islands bar the Palawan group. Notably, though, a smaller form (introduced by Darlington in 1957, used frequently from 1998 onwards) in which all of the Philippine islands are excluded is entrenched within the recent literature, but this is often without evident justification. It should also be recognized that the 'reduced' (=southern) Wallacea area was effectively defined by Heilprin in 1887, but was then labelled the 'Austro-Malaysian Transition Zone'. Finally, the application in recent years of modern analytical techniques has not led to a consensus view on where the lines/areas should run/be placed; with such a large, diverse set of organisms, each with differing histories, this is perhaps not surprising.

Geological data indicate that the interpretation for the age-calibrated phylogeny for the Kurixalus-genus frogs of South, South-east and East Asia (Lv et al., 2018) needs to be rethought.

Recently, Lv et al. (2018) published an age-calibrated phylogenetic tree for the Kurixalus frogs, members of which occur across parts of South, South-east and East Asia. A clade on Taiwan, represented by Kurixalus idiootocus and the Kurixalus eiffingeri species complex, is deemed to have been resident since the middle Cenozoic; its closest congeners are in southern Indochina (not in the adjacent parts of south-east China), and the split between the two is dated at 32.8 Ma. Furthermore, a sub-population of Kurixalus eiffingeri is believed to have colonized islands in the western Ryukyus c. 13.5 Ma. There is, however, a problem with this scenario: the landmass regarded as modern-day Taiwan has existed only for 4-5 million years (it results from a young and ongoing tectonic-plate collision). Assuming the Kurixalus phylogeny and the dating of its branchings are correct, then a palaeobiogeographical scenario involving an older, alternative land surface with later transfer to Taiwan, possibly involving over-water dispersal, would reconcile the biology, but testing this may be difficult/impossible. If the ages of the nodes in the proposed tree are found to be significantly overestimated, the geology and biology might more easily be accommodated.

Global hotspots in the present-day distribution of ancient animal and plant lineages.

The current distribution of biotic lineages that emerged in the deep time has both theoretical and practical implications, in particular for understanding the processes that have forged present-day biodiversity and informing local and regional-scale conservation efforts. To date however, there has been no examination of such patterns globally across taxa and geological time. Here we map the diversity of selected extant seed plant and tetrapod vertebrate lineages that were already in existence either in the latest Triassic or latest Cretaceous. For Triassic-age lineages, we find concentrations in several regions - both tropical and temperate - parts of North America, Europe, East and South-east Asia, northern South America, and New Zealand. With Cretaceous-age lineages, high values are relatively uniformly distributed across the tropics, with peak the values along the Andes, in South-east Asia and Queensland, but also in the temperate Cape Mountains. These patterns result from a combination of factors, including land area, geographic isolation, climate stability and mass extinction survival ability. While the need to protect many of these lineages has been long recognised, a spatially-explicit approach is critical for understanding and maintaining the factors responsible for their persistence, and this will need to be taken forward across finer scales.

Miocene Shark and Batoid Fauna from Nosy Makamby (Mahajanga Basin, Northwestern Madagascar).

Madagascar is well known for producing exceptional fossils. However, the record for selachians remains relatively poorly known. Paleontological reconnaissance on the island of Nosy Makamby, off northwest Madagascar, has produced a previously undescribed assemblage of Miocene fossils. Based on isolated teeth, ten taxonomic groups are identified: Otodus, Carcharhinus, Galeocerdo, Rhizoprionodon, Sphyrna, Hemipristis, Squatina, Rostroraja, Himantura and Myliobatidae. Six are newly described from Madagascar for the Cenozoic (Galeocerdo, Rhizoprionodon, Sphyrna, Squatina, Rostroraja and Himantura). In association with these specimens, remains of both invertebrates (e.g., corals, gastropods, bivalves) and vertebrates (e.g., bony fish, turtles, crocodylians, and sirenian mammals) were also recovered. The sedimentary facies are highly suggestive of a near-shore/coastal plain depositional environment. This faunal association shares similarities to contemporaneous sites reported from North America and Europe and gives a glimpse into the paleoenvironment of Madagascar's Miocene, suggesting that this region was warm, tropical shallow-water marine.

Imperfect isolation: factors and filters shaping Madagascar's extant vertebrate fauna.

Analyses of phylogenetic topology and estimates of divergence timing have facilitated a reconstruction of Madagascar's colonization events by vertebrate animals, but that information alone does not reveal the major factors shaping the island's biogeographic history. Here, we examine profiles of Malagasy vertebrate clades through time within the context of the island's paleogeographical evolution to determine how particular events influenced the arrival of the island's extant groups. First we compare vertebrate profiles on Madagascar before and after selected events; then we compare tetrapod profiles on Madagascar to contemporary tetrapod compositions globally. We show that changes from the Mesozoic to the Cenozoic in the proportions of Madagascar's tetrapod clades (particularly its increase in the representation of birds and mammals) are tied to changes in their relative proportions elsewhere on the globe. Differences in the representation of vertebrate classes from the Mesozoic to the Cenozoic reflect the effects of extinction (i.e., the non-random susceptibility of the different vertebrate clades to purported catastrophic global events 65 million years ago), and new evolutionary opportunities for a subset of vertebrates with the relatively high potential for transoceanic dispersal potential. In comparison, changes in vertebrate class representation during the Cenozoic are minor. Despite the fact that the island's isolation has resulted in high vertebrate endemism and a unique and taxonomically imbalanced extant vertebrate assemblage (both hailed as testimony to its long isolation), that isolation was never complete. Indeed, Madagascar's extant tetrapod fauna owes more to colonization during the Cenozoic than to earlier arrivals. Madagascar's unusual vertebrate assemblage needs to be understood with reference to the basal character of clades originating prior to the K-T extinction, as well as to the differential transoceanic dispersal advantage of other, more recently arriving clades. Thus, the composition of Madagascar's endemic vertebrate assemblage itself provides evidence of the island's paleogeographic history.

Spatial and temporal arrival patterns of Madagascar's vertebrate fauna explained by distance, ocean currents, and ancestor type.

How, when, and from where Madagascar's vertebrates arrived on the island is poorly known, and a comprehensive explanation for the distribution of its organisms has yet to emerge. We begin to break that impasse by analyzing vertebrate arrival patterns implied by currently existing taxa. For each of 81 clades, we compiled arrival date, source, and ancestor type (obligate freshwater, terrestrial, facultative swimmer, or volant). We analyzed changes in arrival rates, with and without adjusting for clade extinction. Probability of successful transoceanic dispersal is negatively correlated with distance traveled and influenced by ocean currents and ancestor type. Obligate rafters show a decrease in probability of successful transoceanic dispersal from the Paleocene onward, reaching the lowest levels after the mid-Miocene. This finding is consistent with a paleoceanographic model [Ali JR, Huber M (2010) Nature 463:653-656] that predicts Early Cenozoic surface currents periodically conducive to rafting or swimming from Africa, followed by a reconfiguration to present-day flow 15-20 million years ago that significantly diminished the ability for transoceanic dispersal to Madagascar from the adjacent mainland.

Mammalian biodiversity on Madagascar controlled by ocean currents.

Madagascar hosts one of the world's most unusual, endemic, diverse and threatened concentrations of fauna. To explain its unique, imbalanced biological diversity, G. G. Simpson proposed the 'sweepstakes hypothesis', according to which the ancestors of Madagascar's present-day mammal stock rafted there from Africa. This is an important hypothesis in biogeography and evolutionary theory for how animals colonize new frontiers, but its validity is questioned. Studies suggest that currents were inconsistent with rafting to Madagascar and that land bridges provided the migrants' passage. Here we show that currents could have transported the animals to the island and highlight evidence inconsistent with the land-bridge hypothesis. Using palaeogeographic reconstructions and palaeo-oceanographic modelling, we find that strong surface currents flowed from northeast Mozambique and Tanzania eastward towards Madagascar during the Palaeogene period, exactly as required by the 'sweepstakes process'. Subsequently, Madagascar advanced north towards the equatorial gyre and the regional current system evolved into its modern configuration with flows westward from Madagascar to Africa. This may explain why no fully non-aquatic land mammals have colonized Madagascar since the arrival of the rodents and carnivorans during the early-Miocene epoch. One implication is that rafting may be the dominant means of overseas dispersal in the Cenozoic era when palaeocurrent directions are properly considered.

Volcanism, mass extinction, and carbon isotope fluctuations in the Middle Permian of China.

The 260-million-year-old Emeishan volcanic province of southwest China overlies and is interbedded with Middle Permian carbonates that contain a record of the Guadalupian mass extinction. Sections in the region thus provide an opportunity to directly monitor the relative timing of extinction and volcanism within the same locations. These show that the onset of volcanism was marked by both large phreatomagmatic eruptions and extinctions amongst fusulinacean foraminifers and calcareous algae. The temporal coincidence of these two phenomena supports the idea of a cause-and-effect relationship. The crisis predates the onset of a major negative carbon isotope excursion that points to subsequent severe disturbance of the ocean-atmosphere carbon cycle.