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BIOdiversity over Microevolutionary and Macroevolutionary scales: Evolutionary and ecological determinants revisited

Periodic Report Summary 1 - BIOMME (BIOdiversity over Microevolutionary and Macroevolutionary scales: Evolutionary and ecological determinants revisited)

The question ‘What determines patterns of biodiversity over time, space, and groups?’ was the main focus of the Marie Curie IOF (627684, project BIOMME). The non-random variation in species richness among taxonomic groups and across geographic regions is one of the most striking features of life on Earth. Understanding how this species diversity is controlled represents one the 25 key research themes for the future identified in the 125th Anniversary issue of Science. The mechanisms that govern the origin, assembly and evolution of these patterns remain obscure, representing a fascinating but complex challenge for two main reasons. On the one hand, researchers have traditionally focused on two different, (contrasting) taxonomic levels: within species or among species. Evolutionary biologists have long sought to understand the relationship between microevolution (processes ranging from genetic drift to adaptation within species), which can be observed in both nature and the laboratory; and macroevolution (processes above the species level such as speciation, extinction, and dispersal), which occurs over intervals that far exceed the human lifespan. The connection between these processes has become a major source of conflict in biology. A second major challenge has been to determine which factor/s govern biodiversity dynamics at the within and among-species scale: whether biotic (species interactions, ecological traits, environmental niche space) or abiotic, such as abrupt major climatic or geological changes. Sometimes referred as the Red Queen versus Court Jester hypothesis, characterizing the factors that shape biodiversity patterns at micro and macroevolutionary scales leads to the difficulty of integrating multiple layers of data within a common statistical framework, to better gain a clearer picture of how evolutionary changes are produced.
Several hypotheses have been proposed in the last 150 years to identify determinants of biodiversity at both the micro (within-species) and macro (among-species) evolutionary scales. In this Marie Curie proposal, we revisited some key theories of evolution and ecology using an approach that relies on genomic data from individuals to communities, aiming to construct a new framework linking micro and macroevolutionary processes. We maintain that understanding what determines biodiversity requires a major interdisciplinary effort involving people working on each mode of evolution (micro and macro) who have pioneered integrative approaches. Spurred by the work of Prof. Felix Sperling (University of Alberta, Canada) and Prof. Isabel Sanmartín (Real Jardín Botánico, Madrid, Spain), we have used a multidisciplinary phylogenetically-based approach that combines state-of-the-art phylogenetic inference, molecular dating, historical biogeographic reconstructions, and novel macroevolutionary methods exploring diversification rates - as well as additional sources of evidence from fields as diverse as paleontology, paleogeography, and paleoclimate - to address biodiversity dynamics at different scales. By integrating multiple layers of information, this multidisciplinary approach allowed us to address both evolutionary and ecological theories within a common spatio-temporal statistical framework. Doing so provides an opportunity to outperform traditional approaches that have established correlations between environmental variables and species richness, but did not directly consider evolutionary processes or lacked a deep evolutionary timeframe.
We focused on the family Papilionidae (swallowtail butterflies) because they constitute an ideal group for studying micro and macroevolutionary questions and have the advantages of being widespread and easily recognized, making them one of the most comprehensively surveyed groups in the world, which has been instrumental in the development of many ecological and evolutionary theories. We revisited many of these theories by taking advantage of Next Generation Sequencing techniques to build a large genomic dataset. Using the Nextera Illumina® kit and the NextSeq Illumina platform available at the University of Alberta, we have developed a shotgun approach to sequence low-coverage whole genomes. At the end of year 2015, we have produced 40 genomes spanning the whole genus diversity of Papilionidae (at least one genome per genus has been sequenced). Combining the Nextera kit and NextSeq platform allowed us generating 2.57 billion DNA reads of high quality, which represents a mean of 67 million DNA reads per species. Analyses showed an average of 10-20x coverage depth for all nuclear genes selected so far, and an impressive 5000-15000x coverage depth for the mitochondrial genome. To our knowledge, this is the largest, most complete genomic database of Papilionidae produced so far (and probably for any insect group). This approach holds much promise for future work, as we have managed to identify potential areas to improve the technique and the results. This wealth of data will allow us to tackle long-standing questions regarding the origin of swallowtail diversity, their adaptations, their hyper-variable morphology across genera, and their evolutionary trends over time. For instance, whole-genome sequence data will be used to create linkage maps to locate mutations on genes that contribute to population and/or species differentiation. This will open the possibility to discover genes involved directly in species formation and their genetic expression under different environmental settings.
In parallel, we have addressed the macroevolutionary determinants of large-scale patterns of biodiversity. Relying on a newly built time-calibrated phylogeny comprising most swallowtail groups, coupled with a complete dataset of geographic occurrences and ecological traits, we benefited from the development of new powerful analytical tools to (i) estimate speciation and extinction rates over time, and (ii) reconstruct ancestral character states to retrace the geographic origin and the tempo and mode of geographic/ecological diversification. Evolutionary biologists are just beginning to tease apart how these factors interact during the evolution of an organism lineage. In particular, we used the full range of these models - some of them developed by us - to address the macroevolutionary processes that govern biodiversity dynamics and to revisit several theories proposed since the times of Alfred Wallace, using species-level phylogenies of birdwings, Apollo butterflies, and the New World genus Papilio. We investigated (1) the effect of host plant under the theory of insect-plant evolution and the ‘escape-and-radiate’ hypothesis predicting high diversification rates following host plant colonization; (2) the effect of geographical range evolution, by tracking the expansion and contraction of the ranges of swallowtails, using biogeographic reconstructions in order to assess the impact of geological changes; and (3) the role of past environmental changes on diversification using a novel paleoenvironment-dependent macroevolutionary model developed by the fellow to understand the role of changing temperature and altitude over geological time scales on the biodiversity dynamics of birdwing butterflies. Deep-time macroevolutionary analyses, such as those attempted here, can provide invaluable results on the evolutionary response of organisms to major cooling and warming events in the past, as well as on the effect of future climatic changes.