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Based on extensive geographic sampling of morphological, ddRADseq and functional trait data, we have identified eight distinct evolutionary lineages within the putative hyperdominant taxon P. heptaphyllum. We are using a “traditional” species concept—a typological or morphological species concept where we expect different species to have discrete morphological differences but also represent monophyletic groups with limited genetic admixture. Morphological traits overlap at varying levels, but genetic data suggest that this widespread group represents distinct, independently adapted lineages that diverged over the past million years. We refute the hypothesis that P. heptaphyllum s.l. is a single species and instead find evidence for recognizing eight independently evolving species (or lineages, sensu20). Updates regarding the taxonomic treatment within P. heptaphyllum s.l. are in progress (e.g. Protium cordatum Huber sensu21) and detailed descriptions of new species are in preparation as part of a taxonomic revision (Table S2, Figure S2).Even though a large number of new species have been recently described in the Neotropics9,10,22, very few studies have attempted to resolve morphologically challenging species complexes (e.g.,13,15). In the sections below, we discuss the implications of our results in the context of: (i) revisiting the concept of hyperdominance for Amazonian trees, (ii) improving richness and diversity estimates, (iii) understanding diversification within dominant tropical lineages, and (iv) refining predictions for ecosystem function.Implications for the hyperdominance phenomenonThe fact that communities often harbor a small group of demographically abundant species in addition to a much larger number of rare species is not a recent discovery (e.g.,23 as cited in3). This pattern, also called a species oligarchy and hyperdominance, was first reported for western Amazonian forests in the early 2000s24,25 and again on the pan-Amazonian scale based on data from the ATDN, one of the largest tree community datasets ever compiled in the tropics1. Hyperdominant species have captured the imagination of many tropical ecologists. First, they have been thought to be more likely to be correctly identified than rare species22, allowing for people to use them as proxies for ecosystem-wide function. For example, Fauset et al.4 emphasized that hyperdominant species were responsible for half of carbon storage and productivity in the Amazon. Second, ecologists have proposed that hyperdominants have important shared demographic properties—they often have large geographic ranges but are only dominant in one or two regions and are often habitat specialists1. In contrast, our results suggest that the hyperdominant taxon P. heptaphyllum s.l. actually consists of several lineages warranting recognition as new species that have very different functional traits, that occupy distinct geographic ranges, and that can be rare or threatened. We postulate that similar conclusions could be reached with many of the other hyperdominant species, which are also thought to be members of species complexes (e.g., Iriartea deltoidea Ruiz and Pav.26; Eschweilera coriacea (DC.) S.A. Mori27). Further study is warranted prioritizing the study of these putative species complexes to refine our understanding of dominance across tropical regions28. If fewer species are found to be true hyperdominants, this will render conservation efforts and ecosystem modeling exercises more complicated than has been discussed to date.Taxonomic relevanceProtium is one of the best studied plant groups in the Neotropics (e.g.,17,18,19). Currently, the genus consists of approximately 200 species, and their systematics has been studied by a collaborative team of taxonomists and evolutionary biologists. Protium has a wide geographic range of specimen sampling, and genomic data are available for a number of species18,29,30. Also, current species descriptions in Protium are consistently founded on both morphological and molecular phylogenetic evidence19. Furthermore, the broad intraspecific sampling of key lineages/taxa within Protium heptaphyllum s.l. gives us high confidence in our results, in contrast to other plant groups that have not yet been subjected to similar intensive systematic study but often include diverse and abundant trees in the Amazon Basin. Here, we showed that a multidisciplinary effort and relatively short time investment on a hyperdominant species complex (3–5 years) has yielded the discovery of eight new lineages warranting species status.Multiple other tree families are relatively well studied in the Neotropics (e.g., Annonaceae, Sapotaceae, Lecythidaceae, Rubiaceae, Chrysobalanaceae, Fabaceae, Melastomataceae), but are also frequently cited as containing a few species complexes with incomplete genetic divergence and requiring detailed revision (e.g., Eschweilera27, Pouteria31). We acknowledge that the field of taxonomy is dynamic (ter Steege et al. 2019) in the sense that classification and species names are likely to change as new studies are performed. Besides that, the methods applied to describe, re-establish, or invalidate taxonomic entities are frequently inconsistent among taxonomists and experts, and can vary according to several species concepts and definitions32,33. Inconsistency in taxonomic methods has been the focus of recent debates about tree species richness in Amazonia9,10. While the authors of these studies disagreed about the number of Amazonian tree species, both sides agree that there is still much work to be done in order to improve taxonomy and to increase the pace of species discovery22. We propose that the establishment of a consensus prioritized list of other species complexes from putative hyperdominant taxa such as P. heptaphyllum, s.l. would represent a significant step to contribute to efficient progress of new species discovery. With the advent of cheaper and more rapid techniques for both molecular systematics and functional ecology, we expect that interdisciplinary approaches combined with an extensive populational sampling like we have done will be highly beneficial for the study of hyperdominant species complexes and to advance the estimates of Amazonian tree species diversity.Refining the understanding of trait variation and functional responseThe seven distinct lineages for the Central/West Amazon Basin and Northeast Amazonian regions showed substantial variation in leaf and wood traits (Fig. 4). Overall, more than half of the breadth of variation in these functional traits that has been observed across 2600 Amazonian species (e.g.,34,35,36) can be found within this single species complex.Moreover, the breadth of functional trait variation also varied markedly within lineages. The low within-lineage trait variation in the Amazonian TUC (orange) population (Fig. 4) is consistent with adaptation to dry savanna environments; that is, this lineage exhibits consistent high-water use efficiency (less negative 13C) and small, dense xylem vessels. In contrast, the CRS (red) population, which also exhibits low within-lineage functional trait variation, displays values of traits consistent with functional responses to flooding in Amazonian igapó habitats where it is found, and thus has low water use efficiency and large xylem vessels. Together, these lineages contribute to the broad variation observed in the species complex, while at the same time other lineages from Central Brazil and the Atlantic Coast (light and dark blue) show high within-lineage functional trait variation and broad distribution across habitats. Taken together across the phylogeny of the entire species complex, these functional traits can be considered to be highly labile, with some lineages adapting to contrasting extreme values whereas other sister lineages retain broad functional trait variation (Fig. 4).Importantly, this variation is consistent with the evolutionary histories of each distinct lineage within the species complex. For example, the P. heptaphyllum, P. “tucuruiense” and P. “aromaticum” (yellow, orange and blue) clades experienced a relatively recent population bottleneck and then expanded, likely with traits that permitted them to radiate into the drier savanna environments where they were then able to expand (Fig. 2). Some of these lineages have become adapted to distinct habitats and are responding very differently to current environmental conditions. Moreover, we suggest that these lineages will respond very differently to future changes in climatic conditions across the region, with some of them poorly equipped for the predicted increasing frequency and intensity of droughts37.Our results have important implications for ecosystem function. Since the advent of functional trait network studies (e.g., TRY Plant Trait Database38), understanding how plant species behave in terms of their physiological performance over large scales has led to important predictions of the consequences of future scenarios of climate and land-use change39,40,41. The importance of the Amazon region for the global climate and carbon cycle42,43 highlights the need to devote substantial effort to investigating the taxonomy of hyperdominant plant taxa. For instance, if some or most of the hyperdominant taxa actually represent multiple hidden evolutionary entities, as in P. heptaphyllum s.l., a larger fraction of Amazonian tree species would contribute proportionally more to carbon storage and cycling than described by Fauset et al.4, rendering modeling exercises and management much more nuanced. In addition, a comprehensive taxonomic review of dominant tree lineages with concomitant screening of functional traits as we conducted for this species complex, would greatly improve the understanding of climate-induced functional shifts, such as described by Esquivel‐Muelbert et al.41, and have potentially important consequences for the conservation of putative rare taxa that are nested within hyperdominant species complexes.Understanding diversification in dominant lineagesThe scenario of some hyperdominant or oligarchic taxa representing multiple diverged lineages is intriguing and relevant for understanding the processes of diversification in the Amazonian flora. Based on the demographic history of P. heptaphyllum s.l., older lineages tend to be habitat specialists and less morphologically and functionally variable. In contrast, recently evolved lineages have colonized new areas and frequently experience gene flow across very large geographic distances, and they are morphologically and functionally more variable. We hypothesize that large population sizes may be associated with higher diversification rates due to the process of population expansion followed by radiation into different habitats. Therefore, dominant lineages would have better chances to speciate via habitat specialization and generate large clades than non-dominant lineages. Habitat specialization is considered to have evolved in many tropical plant groups44,45 and many different tree genera have become specialized in contrasting environments46.According to our results, P. heptaphyllum s.l. diverged from its common ancestors around five million years ago and diversified first in the Amazon region followed by an increase in population size. Many lineages subsequently became specialized to white-sand habitats, seasonally flooded forests in the Rio Negro Basin (Igapó forests), and floodplain forests (várzea forests). However, more recently, lineages dispersed into neighboring floristic domains (e.g. Cerrado and Atlantic Forest) and ecotone areas, colonizing regions where the annual precipitation is currently lower and seasonal. These populations found in Central and Coastal Brazil are genetically very similar to each other despite the large geographical distances among them. Moreover, these populations are functionally more variable than the early-diverging lineages in the Amazon. In contrast, older lineages from the Amazon basin were found to be less morphologically plastic and more isolated in terms of gene flow. White-sand ecosystems in Amazonia are characterized by a patchy and geographically disjunct distribution47 that could have inhibited dispersal of habitat-specialist populations, resulting in repeated speciation in white-sand forests in different regions.Conservation implicationsWe show that at least four newly discovered lineages, including two “resurrected” species, are geographically restricted, demographically rare and endemic to white-sand vegetation in the Amazon (e.g. P. cordatum sensu Damasco et al. 2019a, P. “tucuruiense,” P. angustifolium Swart, and P. “reticuliflorum”). Future studies aiming to review potential species complexes among hyperdominant species could indicate other threatened lineages warranting taxonomic recognition as well as new geographic areas for conservation priority. While many studies have relied on datasets compiled by plot-inventory networks, more effort should be focused on increasing the pace of taxonomic research in the Neotropics22,28. Deforestation rates in Amazonia are likely to increase in the next few years; and yet one third of the total number of tree species are likely still undescribed or undiscovered1.We believe that reports that roughly half of all biomass and carbon storage in one of the most diverse areas on Earth is stored by a very small group of “hyperdominant” species may be misinforming policy makers and stakeholders. Based on our integrative review of P. heptaphyllum s.l., we showed that genetic diversity and functional responses to environmental gradients are much greater than expected by the hyperdominance principle. Our results revealed that a single “hyperdominant” taxon contains several lineages warranting recognition as distinct species that include great functional diversity, including at least three that are relatively rare and potentially threatened. Metapopulations of a hyperdominant taxon may be interpreted as much more resilient to future global changes than relatively rare lineages within a species complex. Thus, our findings suggest not only critical issues with species level conservation for lineages that should now be considered threatened taxa and not hyper- nor dominant, but also that some of these putatively new lineages might be at risk of extinction due to future climate change and increasing deforestation. Although the distinction between species and population delimitation may not be of consequence for calculating current carbon storage, we argue that multiple distinct lineages with limited gene flow such as we describe here will likely respond very differently to current and future global changes than a larger interbreeding metapopulation of a single lineage. We therefore caution against simplistic assumptions about biogeochemical processes and ecosystem services reliant on the attractive simplicity of a putative hyperdominance phenomenon. More

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