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Explaining broad molecular, phenotypic and species biodiversity patterns necessitates a unifying framework spanning multiple evolutionary scales. Here we argue that although substantial effort has been made to reconcile microevolution and macroevolution, much work remains to identify the links between biological processes at play. We highlight four major questions of evolutionary biology whose solutions require conceptual bridges between micro and macroevolution. We review potential avenues for future research to establish how mechanisms at one scale (drift, mutation, migration, selection) translate to processes at the other scale (speciation, extinction, biogeographic dispersal) and vice versa. We propose ways in which current comparative methods to infer molecular evolution, phenotypic evolution and species diversification could be improved to specifically address these questions. We conclude that researchers are in a better position than ever before to build a synthesis to understand how microevolutionary dynamics unfold over millions of years. 

BACKGROUND Madagascar is one of the world’s foremost biodiversity hotspots. Its unique assemblage of plants, animals, and fungi—the majority of which evolved on the island and occur nowhere else—is both diverse and threatened. After human arrival, the island’s entire megafauna became extinct, and large portions of the current flora and fauna may be on track for a similar fate. Conditions for the long-term survival of many Malagasy species are not currently met because of multiple anthropogenic threats. ADVANCES We review the extinction risk and threats to biodiversity in Madagascar, using available international assessment data as well as a machine learning analysis to predict the extinction risks and threats to plant species lacking assessments. Our compilation of global International Union for Conservation of Nature (IUCN) Red List assessments shows that overexploitation alongside unsustainable agricultural practices affect 62.1 and 56.8% of vertebrate species, respectively, and each affects nearly 90% of all plant species. Other threats have a relatively minor effect today but are expected to increase in coming decades. Because only one-third (4652) of all Malagasy plant species have been formally assessed, we carried out a neural network analysis to predict the putative status and threats for 5887 unassessed species and to evaluate biases in current assessments. The percentage of plant species currently assessed as under threat is probably representative of actual numbers, except in the case of the ferns and lycophytes, where significantly more species are estimated to be threatened. We find that Madagascar is home to a disproportionately high number of Evolutionarily Distinct and Globally Endangered (EDGE) species. This further highlights the urgency for evidence-based and effective in situ and ex situ conservation. Despite these alarming statistics and trends, we find that 10.4% of Madagascar’s land area is protected and that the network of protected areas (PAs) covers at least part of the range of 97.1% of terrestrial and freshwater vertebrates with known distributions (amphibians, freshwater fishes, reptiles, birds, and mammal species combined) and 67.7% of plant species (for threatened species, the percentages are 97.7% for vertebrates and 79.6% for plants). Complementary to this, ex situ collections hold 18% of vertebrate species and 23% of plant species. Nonetheless, there are still many threatened species that do not occur within PAs and are absent from ex situ collections, including one amphibian, three mammals, and seven reptiles, as well as 559 plants and more yet to be assessed. Based on our updated vegetation map, we find that the current PA network provides good coverage of the major habitats, particularly mangroves, spiny forest, humid forest, and tapia, but subhumid forest and grassland-woodland mosaic have very low areas under protection (5.7 and 1.8% respectively). OUTLOOK Madagascar is among the world’s poorest countries, and its biodiversity is a key resource for the sustainable future and well-being of its citizens. Current threats to Madagascar’s biodiversity are deeply rooted in historical and present social contexts, including widespread inequalities. We therefore propose five opportunities for action to further conservation in a just and equitable way. First, investment in conservation and restoration must be based on evidence and effectiveness and be tailored to meet future challenges through inclusive solutions. Second, expanded biodiversity monitoring, including increased dataset production and availability, is key. Third, improving the effectiveness of existing PAs—for example through community engagement, training, and income opportunities—is more important than creating new ones. Fourth, conservation and restoration should not focus solely on the PA network but should also include the surrounding landscapes and communities. And finally, conservation actions must address the root causes of biodiversity loss, including poverty and food insecurity. In the eyes of much of the world, Madagascar’s biodiversity is a unique global asset that needs saving; in the daily lives of many of the Malagasy people, it is a rapidly diminishing source of the most basic needs for subsistence. Protecting Madagascar’s biodiversity while promoting social development for its people is a matter of the utmost urgency Visual representation of five key opportunities for conserving and restoring Madagascar’s rapidly declining biodiversity identified in this Review. The dashed lines point to representative vegetation types where these recommendations could have tangible effects, but the opportunities are applicable across Madagascar. ILLUSTRATION: INESSA VOET 

BACKGROUND The Republic of Madagascar is home to a unique assemblage of taxa and a diverse set of ecosystems. These high levels of diversity have arisen over millions of years through complex processes of speciation and extinction. Understanding this extraordinary diversity is crucial for highlighting its global importance and guiding urgent conservation efforts. However, despite the detailed knowledge that exists on some taxonomic groups, there are large knowledge gaps that remain to be filled. ADVANCES Our comprehensive analysis of major taxonomic groups in Madagascar summarizes information on the origin and evolution of terrestrial and freshwater biota, current species richness and endemism, and the utilization of this biodiversity by humans. The depth and breadth of Madagascar’s biodiversity—the product of millions of years of evolution in relative isolation —is still being uncovered. We report a recent acceleration in the scientific description of species but many remain relatively unknown, particularly fungi and most invertebrates. DIGITIZATION Digitization efforts are already increasing the resolution of species richness patterns and we highlight the crucial role of field- and collections-based research for advancing biodiversity knowledge in Madagascar. Phylogenetic diversity patterns mirror that of species richness and endemism in most of the analyzed groups. Among the new data presented, our update on plant numbers estimates 11,516 described vascular plant species native to Madagascar, of which 82% are endemic, in addition to 1215 bryophyte species, of which 28% are endemic. Humid forests are highlighted as centers of diversity because of their role as refugia and centers of recent and rapid radiations, but the distinct endemism of other areas such as the grassland-woodland mosaic of the Central Highlands and the spiny forest of the southwest is also important despite lower species richness. Endemism in Malagasy fungi remains poorly known given the lack of data on the total diversity and global distribution of species. However, our analysis has shown that ~75% of the fungal species detected by environmental sequencing have not been reported as occurring outside of Madagascar. Among the 1314 species of native terrestrial and freshwater vertebrates, levels of endemism are extremely high (90% overall)—all native nonflying terrestrial mammals and native amphibians are found nowhere else on Earth; further, 56% of the island’s birds, 81% of freshwater fishes, 95% of mammals, and 98% of reptile species are endemic. Little is known about endemism in insects, but data from the few well-studied groups on the island suggest that it is similarly high. The uses of Malagasy species are many, with much potential for the uncovering of useful traits for food, medicine, and climate mitigation. OUTLOOK Considerable work remains to be done to fully characterize Madagascar’s biodiversity and evolutionary history. The multitudes of known and potential uses of Malagasy species reported here, in conjunction with the inherent value of this unique and biodiverse region, reinforce the importance of conserving this unique biota in the face of major threats such as habitat loss and overexploitation. The gathering and analysis of data on Madagascar’s remarkable biota must continue and accelerate if we are to safeguard this unique and highly threatened subset of Earth’s biodiversity. Emergence and composition of Madagascar’s extraordinary biodiversity. Madagascar’s biota is the result of over 160 million years of evolution, mostly in geographic isolation, combined with sporadic long distance immigration events and local extinctions. (Left) We show the age of the oldest endemic Malagasy clade for major groups (from bottom to top): arthropods, bony fishes, reptiles, flatworms, birds, amphibians, flowering plants, mammals, non-flowering vascular plants, and mollusks). Humans arrived recently, some 10,000 to 2000 years (top right) and have directly or indirectly caused multiple extinctions (including hippopotamus, elephant birds, giant tortoises, and giant lemurs) and introduced many new species (such as dogs, zebu, rats, African bushpigs, goats, sheep, rice). Endemism is extremely high and unevenly distributed across the island (the heat map depicts Malagasy palm diversity, a group characteristic of the diverse humid forest). Human use of biodiversity is widespread, including 1916 plant species with reported uses. The scientific description of Malagasy biodiversity has accelerated greatly in recent years (bottom right), yet the diversity and evolution of many groups remain practically unknown, and many discoveries await. 

The end-Cretaceous event was catastrophic for terrestrial communities worldwide, yet its long-lasting effect on tropical forests remains largely unknown. We quantified plant extinction and ecological change in tropical forests resulting from the end-Cretaceous event using fossil pollen (>50,000 occurrences) and leaves (>6000 specimens) from localities in Colombia. Late Cretaceous (Maastrichtian) rainforests were characterized by an open canopy and diverse plant–insect interactions. Plant diversity declined by 45% at the Cretaceous–Paleogene boundary and did not recover for ~6 million years. Paleocene forests resembled modern Neotropical rainforests, with a closed canopy and multistratal structure dominated by angiosperms. The end-Cretaceous event triggered a long interval of low plant diversity in the Neotropics and the evolutionary assembly of today’s most diverse terrestrial ecosystem.

 

Linking pattern to process across spatial and temporal scales has been a key goal of the field of biogeography. In January 2017, the 8th biennial conference of the International Biogeography Society sponsored a symposium onBuilding up biogeography—process to patternthat aimed to review progress towards this goal. Here we present a summary of the symposium, in which we identified promising areas of current research and suggested future research directions. We focus on (1) emerging types of data such as behavioural observations and ancientDNA, (2) how to better incorporate historical data (such as fossils) to move beyond what we term “footprint measures” of past dynamics and (3) the role that novel modelling approaches (e.g. maximum entropy theory of ecology and approximate Bayesian computation) and conceptual frameworks can play in the unification of disciplines. We suggest that the gaps separating pattern and process are shrinking, and that we can better bridge these aspects by considering the dimensions of space and time simultaneously.

 

Species interactions lie at the heart of many theories of macroevolution, from adaptive radiation to the Red Queen. Although some theories describe the imprint that interactions will have over long timescales, we are still missing a comprehensive understanding of the effects of interactions on macroevolution. Current research shows strong evidence for the impact of interactions on macroevolutionary patterns of trait evolution and diversification, yet many macroevolutionary studies have only a tenuous relationship to ecological studies of interactions over shorter timescales. We review current research in this area, highlighting approaches that explicitly model species interactions and connect them to broad‐scale macroevolutionary patterns. We also suggest that progress has been made by taking an integrative interdisciplinary look at individual clades. We focus on African cichlids as a case study of how this approach can be fruitful. Overall, although the evidence for species interactions shaping macroevolution is strong, further work using integrative and model‐based approaches is needed to spur progress towards understanding the complex dynamics that structure communities over time and space.