Isabel Sanmartín

Amazonia Through Time: Andean Uplift, Climate Change, Landscape Evolution, and Biodiversity

The Making of Amazonian Diversity The biodiversity of the Amazon Basin is legendary, but the processes by which it has been generated have been debated. In the late 20th century the prevalent view was that the engine of diversity was repeated contraction and expansion of forest refugia during the past 3 million years or so. Hoorn et al. (p. 927) analyze findings from a diverse range of disciplines, including molecular phylogeny, ecology, sedimentology, structural geology, and palaeontology, to offer an overview of the entire history of this region during the Cenozoic era (66 million years ago). The uplift of the Andes was a pivotal event in the evolution of Amazonian landscapes because it continually altered river drainage patterns, which in turn put a variety of pressures on organisms to adapt to changing conditions in a multiplicity of ways. Hence, the diversity of the modern biota of the Amazon has more ancient origins than previously thought. The Amazonian rainforest is arguably the most species-rich terrestrial ecosystem in the world, yet the timing of the origin and evolutionary causes of this diversity are a matter of debate. We review the geologic and phylogenetic evidence from Amazonia and compare it with uplift records from the Andes. This uplift and its effect on regional climate fundamentally changed the Amazonian landscape by reconfiguring drainage patterns and creating a vast influx of sediments into the basin. On this “Andean” substrate, a region-wide edaphic mosaic developed that became extremely rich in species, particularly in Western Amazonia. We show that Andean uplift was crucial for the evolution of Amazonian landscapes and ecosystems, and that current biodiversity patterns are rooted deep in the pre-Quaternary.

Tracing the impact of the Andean uplift on Neotropical plant evolution.

Recent phylogenetic studies have revealed the major role played by the uplift of the Andes in the extraordinary diversification of the Neotropical flora. These studies, however, have typically considered the Andean uplift as a single, time-limited event fostering the evolution of highland elements. This contrasts with geological reconstructions indicating that the uplift occurred in discrete periods from west to east and that it affected different regions at different times. We introduce an approach for integrating Andean tectonics with biogeographic reconstructions of Neotropical plants, using the coffee family (Rubiaceae) as a model group. The distribution of this family spans highland and montane habitats as well as tropical lowlands of Central and South America, thus offering a unique opportunity to study the influence of the Andean uplift on the entire Neotropical flora. Our results suggest that the Rubiaceae originated in the Paleotropics and used the boreotropical connection to reach South America. The biogeographic patterns found corroborate the existence of a long-lasting dispersal barrier between the Northern and Central Andes, the “Western Andean Portal.” The uplift of the Eastern Cordillera ended this barrier, allowing dispersal of boreotropical lineages to the South, but gave rise to a huge wetland system (“Lake Pebas”) in western Amazonia that prevented in situ speciation and floristic dispersal between the Andes and Amazonia for at least 6 million years. Here, we provide evidence of these events in plants.

Accounting for Phylogenetic Uncertainty in Biogeography: A Bayesian Approach to Dispersal-Vicariance Analysis of the Thrushes (Aves: Turdus)

The phylogeny of the thrushes (Aves: Turdus) has been difficult to reconstruct due to short internal branches and lack of node support for certain parts of the tree. Reconstructing the biogeographic history of this group is further complicated by the fact that current implementations of biogeographic methods, such as dispersal-vicariance analysis (DIVA; Ronquist, 1997), require a fully resolved tree. Here, we apply a Bayesian approach to dispersal-vicariance analysis that accounts for phylogenetic uncertainty and allows a more accurate analysis of the biogeographic history of lineages. Specifically, ancestral area reconstructions can be presented as marginal distributions, thus displaying the underlying topological uncertainty. Moreover, if there are multiple optimal solutions for a single node on a certain tree, integrating over the posterior distribution of trees often reveals a preference for a narrower set of solutions. We find that despite the uncertainty in tree topology, ancestral area reconstructions indicate that the Turdus clade originated in the eastern Palearctic during the Late Miocene. This was followed by an early dispersal to Africa from where a worldwide radiation took place. The uncertainty in tree topology and short branch lengths seems to indicate that this radiation took place within a limited time span during the Late Pliocene. The results support the role of Africa as a probable source area for intercontinental dispersals as suggested for other passerine groups, including basal diversification within the songbird tree.

Reconstructing the Evolution and Biogeographic History of Tribe Cardueae (Compositae)

UNLABELLED PREMISE OF THE STUDY Tribe Cardueae (thistles) forms one of the largest tribes in the family Compositae (2400 species), with representatives in almost every continent. The greatest species richness of Cardueae occurs in the Mediterranean region where it forms an important element of its flora. New fossil evidence and a nearly resolved phylogeny of Cardueae are used here to reconstruct the spatiotemporal evolution of this group. • METHODS We performed maximum parsimony and Bayesian phylogenetic inference based on nuclear ribosomal DNA and chloroplast DNA markers. Divergence times and ancestral area reconstructions for main lineages were estimated using penalized likelihood and dispersal-vicariance analyses, respectively, and integrated over the posterior distribution of the phylogeny from the Bayesian Markov chain Monte Carlo analysis to accommodate uncertainty in phylogenetic relationships. • KEY RESULTS The phylogeny shows that subtribe Cardopatiinae is sister to the remaining subtribes, and subtribes Carlininae and Echinopsinae appear as consecutive sister-clades to the Carduinae/Centaureinae. Tribe Cardueae is inferred to have originated around the Mid Eocene in West Asia, which is also the ancestral area of most subtribes within Cardueae. Diversification within each subtribe began during the Oligocene-Miocene period. • CONCLUSIONS Most diversification events within Cardueae are related to the continuous cycles of area connection and division between the Anatolian microplate and the western Mediterranean Basin during the Oligocene-Miocene and with the uplift of the Himalayan range from the Miocene onward. From these two regions, thistles dispersed and colonized the rest of the continents (e.g., the New World, Africa, and Australia), most likely during the colder Pliocene-Pleistocene period.

Reconstructing the history of Campanulaceae with a Bayesian approach to molecular dating and dispersal–vicariance analyses

We reconstruct here the spatial and temporal evolution of the Campanula alliance in order to better understand its evolutionary history. To increase phylogenetic resolution among major groups (Wahlenbergieae-Campanuleae), new sequences from the rbcL region were added to the trnL-F dataset obtained in a previous study. These phylogenies were used to infer ancestral areas and divergence times in Campanula and related genera using a Bayesian approach to molecular dating and dispersal-vicariance analyses that takes into account phylogenetic uncertainty. The new phylogenetic analysis confirms Platycodoneae as the sister group of Wahlenbergieae-Campanuleae, the two last ones inter-graded into a well-supported clade. Biogeographic and dating analyses suggest that Western Asia and the Eastern Mediterranean have played a major role as centers of migration and diversification within the Campanula alliance, probably in relation to the intense orogenic activity that took place in this region during the Late Neogene, and that could have promoted isolation and allopatric speciation within lineages. Diversification rates within several Campanula lineages would have increased at the end of the Miocene, coinciding with the Messinian Stage. Strong selective pressures from climate changes and the expansion of mountainous regions during this period are suggested to explain the adaptation to drought, cold or disturbed environments observed in many Campanula species. Several independent long-distance dispersal events to North America are inferred within the Rapunculus clade, which seem to be related to high ploidy levels.

Bayesian island biogeography in a continental setting: the Rand Flora case

We here explore the use of a Bayesian approach to island biogeography for disentangling the evolutionary origins of a continental-scale floristic pattern, the enigmatic ‘Rand Flora’. The existence of disjunct distributions across many plant lineages between Macaronesia–northwest Africa, Horn of Africa–southern Arabia and east–south Africa has long intrigued botanists, but only now can we start analysing it within a statistical framework. Phylogenetic and distributional data from 13 plant lineages exhibiting this disjunct distribution were analysed to estimate area carrying capacities and historical rates of biotic exchange between areas. The results indicate that there has been little exchange between southern Africa and the northern African region, and that this exchange occurred via east Africa. Northwest Africa–Macaronesia shows the smallest carrying capacity but highest dispersal rate with other regions, suggesting that its flora was built up by immigration of lineages, probably from the Mediterranean region and western Asia. In contrast, southern Africa shows the highest carrying capacity and lowest dispersal rate, suggesting a flora formed by in situ diversification. We discuss further improvements of the method for addressing more complex hypotheses, such as asymmetric dispersal between regions or repeated cyclical events.

Integrating Fossils, Phylogenies, and Niche Models into Biogeography to Reveal Ancient Evolutionary History: The Case of Hypericum (Hypericaceae)

In disciplines such as macroevolution that are not amenable to experimentation, scientists usually rely on current observations to test hypotheses about historical events, assuming that “the present is the key to the past.” Biogeographers, for example, used this assumption to reconstruct ancestral ranges from the distribution of extant species. Yet, under scenarios of high extinction rates, the biodiversity we observe today might not be representative of the historical diversity and this could result in incorrect biogeographic reconstructions. Here, we introduce a new approach to incorporate into biogeographic inference the temporal, spatial, and environmental information provided by the fossil record, as a direct evidence of the extinct biodiversity fraction. First, inferences of ancestral ranges for those nodes in the phylogeny calibrated with the fossil record are constrained to include the geographic distribution of the fossil. Second, we use fossil distribution and past climate data to reconstruct the climatic preferences and potential distribution of ancestral lineages over time, and use this information to build a biogeographic model that takes into account “ecological connectivity” through time. To show the power of this approach, we reconstruct the biogeographic history of the large angiosperm genus Hypericum, which has a fossil record extending back to the Early Cenozoic. Unlike previous reconstructions based on extant species distributions, our results reveal that Hypericum stem lineages were already distributed in the Holarctic before diversification of its crown-group, and that the geographic distribution of the genus has been relatively stable throughout the climatic oscillations of the Cenozoic. Geographical movement was mediated by the existence of climatic corridors, like Beringia, whereas the equatorial tropical belt acted as a climatic barrier, preventing Hypericum lineages to reach the southern temperate regions. Our study shows that an integrative approach to historical biogeography—that combines sources of evidence as diverse as paleontology, ecology, and phylogenetics—could help us obtain more accurate reconstructions of ancient evolutionary history. It also reveals the confounding effect different rates of extinction across regions have in biogeography, sometimes leading to ancestral areas being erroneously inferred as recent colonization events.

Ancient vicariance and climate-driven extinction explain continental-wide disjunctions in Africa: the case of the Rand Flora genus Canarina (Campanulaceae)

Transoceanic distributions have attracted the interest of scientists for centuries. Less attention has been paid to the evolutionary origins of ‘continent‐wide’ disjunctions, in which related taxa are distributed across isolated regions within the same continent. A prime example is the ‘Rand Flora’ pattern, which shows sister taxa disjunctly distributed in the continental margins of Africa. Here, we explore the evolutionary origins of this pattern using the genus Canarina, with three species: C. canariensis, associated with the Canarian laurisilva, and C. eminii and C. abyssinica, endemic to the Afromontane region in East Africa, as case study. We infer phylogenetic relationships, divergence times and the history of migration events within Canarina using Bayesian inference on a large sample of chloroplast and nuclear sequences. Ecological niche modelling was employed to infer the climatic niche of Canarina through time. Dating was performed with a novel nested approach to solve the problem of using deep time calibration points within a molecular dataset comprising both above‐species and population‐level sampling. Results show C. abyssinica as sister to a clade formed by disjunct C. eminii and C. canariensis. Miocene divergences were inferred among species, whereas infraspecific divergences fell within the Pleistocene–Holocene periods. Although C. eminii and C. canariensis showed a strong genetic geographic structure, among‐population divergences were older in the former than in the latter. Our results suggest that Canarina originated in East Africa and later migrated across North Africa, with vicariance and aridification‐driven extinction explaining the 7000 km/7 million year divergence between the Canarian and East African endemics.

Palaeo-islands as refugia and sources of genetic diversity within volcanic archipelagos: the case of the widespread endemic Canarina canariensis (Campanulaceae)

Geographical isolation by oceanic barriers and climatic stability has been postulated as some of the main factors driving diversification within volcanic archipelagos. However, few studies have focused on the effect that catastrophic volcanic events have had on patterns of within‐island differentiation in geological time. This study employed data from the chloroplast (cpDNA haplotypes) and the nuclear (AFLPs) genomes to examine the patterns of genetic variation in Canarina canariensis, an iconic plant species associated with the endemic laurel forest of the Canary Islands. We found a strong geographical population structure, with a first divergence around 0.8 Ma that has Tenerife as its central axis and divides Canarian populations into eastern and western clades. Genetic diversity was greatest in the geologically stable ‘palaeo‐islands’ of Anaga, Teno and Roque del Conde; these areas were also inferred as the ancestral location of migrant alleles towards other disturbed areas within Tenerife or the nearby islands using a Bayesian approach to phylogeographical clustering. Oceanic barriers, in contrast, appear to have played a lesser role in structuring genetic variation, with intra‐island levels of genetic diversity larger than those between‐islands. We argue that volcanic eruptions and landslides after the merging of the palaeo‐islands 3.5 Ma played key roles in generating genetic boundaries within Tenerife, with the palaeo‐islands acting as refugia against extinction, and as cradles and sources of genetic diversity to other areas within the archipelago.

Historical Biogeography: Evolution in Time and Space

Biogeography is the discipline of biology that studies the present and past distribution patterns of biological diversity and their underlying environmental and historical causes. For most of its history, biogeography has been divided into proponents of vicariance explanations, who defend that distribution patterns can mainly be explained by geological, tectonic-isolating events; and dispersalists, who argue that current distribution patterns are largely the result of recent migration events. This paper provides an overview of the evolution of the discipline from methods focused on finding general patterns of distribution (cladistic biogeography), to those that integrate biogeographic processes (event-based biogeography), to modern probabilistic approaches (parametric biogeography). The latter allows incorporating into biogeographic inference estimates of the divergence time between lineages (usually based on DNA sequences) and external sources of evidence, such as information on past climate and geography, the organism fossil record, or its ecological tolerance. This has revolutionized the discipline, allowing it to escape the dispersal versus vicariance dilemma and to address a wider range of evolutionary questions, including the role of ecological and historical factors in the construction of biomes or the existence of contrasting patterns of range evolution in animals and plants.