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  1. Author Response

    Reviewer #1 (Public Review):

    This paper address the "origins and drivers of Neotropical diversity." The Neotropics have high diversity of plants and animals relative to other global regions. There are also many hotspots of global biodiversity (species richness) within the Neotropics.

    This paper aggregates 150 time-calibrated phylogenies from different groups of plants and animals that occur predominantly in the Neotropics. They analyze the diversification dynamics of these clades over time primarily using the method of Morlon et al. (2011; PNAS) as implemented in RPANDA (Morlon et al. 2016). The authors find that most clades have constant rates of speciation and extinction over time.

    Thank you for having reviewed our study and for your feedback.

    The strength of the paper is that it aggregates many previously published phylogenies of Neotropical organisms. However, it is unclear whether the method used gives meaningful inferences about diversification dynamics over time (e.g. Burin et al. 2019; Syst. Biol.). Therefore, the overall contribution of the study is somewhat questionable.

    This is a legitimate comment, and we understand the skepticism on a study that relies on macroevolutionary models of questionable robustness (e.g. Kubo & Iwasa 1995 - Evolution; Rabosky & Lovette 2008 - Evolution; Crisp & Cook 2009 - Evolution; Quental & Marshall 2010 - TREE; Burin et al. 2019 - Syst. Biol.; Louca & Pennell 2020 - Nature; Pannetier et al. 2021 - Evolution).

    The methodology used here has been thoroughly tested with both simulations (e.g. Morlon et al. 2011 - PNAS; Lewitus & Morlon 2018 - Syst. Biol.; Condamine et al. 2019 - Ecol. Lett.) and empirical cases (e.g. Lewitus et al. 2018 - Nat. Ecol. Evol.; Condamine et al. 2019 - Ecol. Lett.). We cannot deny that such a methodology is fully free from issues, which affect all birth-death models, and brings the question: are we able to reliably infer the diversification model and identify parameter values of this model (Louca & Pennell 2020 - Nature)? These concerns are not likely to be resolved in the short term. Although many studies are making progress in understanding the behavior of diversification rate functions, showing, for example, that equally likely diversification functions (i.e. the congruent parameter space of Louca & Pennell 2020 - Nature) can share common features, with diversification rate patterns being robust despite non-identifiability (Höhna et al., 2022 - bioRxiv; Morlon et al., 2022 - TREE).

    Being aware of these concerns, we also relied on the recently developed Pulled Diversification Rates method (Louca & Pennell 2020 – Nature; Louca et al., 2018 - PNAS) that is supposed to correct for the identifiability issue raised by recent studies. Hence, applying both traditional and pulled birth-death models to all phylogenies, we have shown a good consistency in the inferred models, which suggests that our study can provide meaningful estimates of diversification. Our empirical study is also one of the first to perform such a large-scale methodological comparison in diversification analyses (pulled vs. traditional birth-death models) while addressing a key question in evolutionary biology. We have now emphasized this point in the conclusions of our study: “To the extent possible, these results are based on traditional diversification rates, and on the recently developed Pulled Diversification Rates method that is supposed to correct for the identifiability issue raised by recent studies associated with traditional diversification rates (71). Hence, applying both traditional and pulled birth-death models to all phylogenies, we have shown a good consistency in the inferred models, which suggests that our study can provide meaningful estimates of diversification”.

    The design of the study is also somewhat problematic. There is no comparison to other regions outside the Neotropics, so the study cannot address why the Neotropics are so diverse relative to other continental regions. Similarly, within the Neotropics, the authors do not find significant differences in diversification rates or dynamics among regions. As far as I can tell, they do not attempt to relate patterns of diversification to patterns of species richness among regions within the Neotropics (and presumably they would find no significant patterns if they did).

    We agree with this remark. We are sorry for this confusion. Our study does not aim at addressing why the Neotropics are more diverse than other regions in the world. We simply wanted to establish that the Neotropics are the richest region in the world based on previous studies, and that we are interested in understanding what are the patterns/drivers behind such a diversity. In the Introduction, we state that such diversity is not evenly distributed within the Neotropics, and that some regions are richer (e.g. Andes) than others (e.g. southern cone of South America). Diversity models, from Stebbins (1974), have long been proposed to explain this unbalanced diversity. Our study has then defined different bioregions within the Neotropics in which we have looked for differences in diversification patterns. In other words, we do “attempt to relate patterns of diversification to patterns of species richness among regions within the Neotropics”, although we were not able to explain the observed differences in species richness by differences in diversification dynamics (i.e. diversification dynamics are similar across regions). Please, see our response to the essential revision point 1 addressing this comment.

    In the revised version, we have changed the title of the study as: “Diversification dynamics of plants and tetrapods in the Neotropics through time, clades and biogeographic regions”. We hope you will find this new title better fits the content of the article. In addition, to avoid any confusion in light of your comment, we have deleted the following sentence from the introduction: “But such an assessment is required to understand the origin of Neotropical diversity and why the Neotropics are more diverse than other regions in the world”.

    The authors set up their study by claiming that most previous attempts to explain Neotropical diversity relied on two evolutionary models: cradles vs. museums of diversity. The justification cited for this thinking comes mostly from papers from the last century or before. I do not think that this represents the cutting edge of modern thinking about this topic. Many researchers moved on from this dichotomy long ago.

    Thank you for this interesting comment. You are right. The cradle and museum models of diversity are indeed old definitions (Stebbins 1974 - Flowering Plants: Evolution Above the Species Level), but they were convenient to formulate clear and testable hypotheses on the processes underlying the observed patterns of diversity that Stebbins described. We agree that Stebbins’ view is likely outdated, and that is why we took advantage of these models to draw a series of hypotheses relying on evolutionary processes, which has been argued as a “cutting edge of modern thinking about this topic” (Vasconcelos et al. 2022 - Am. Nat.). In the revised version, we have extended the explanation for our rationale to rely on Stebbins’ models and propose process-based hypotheses to explain diversity patterns. We also cite Vasconcelos et al. (2022 - Am. Nat.). We have modified the introduction as follows: “Although the concepts of cradle and museum have contributed to stimulate numerous macroevolutionary studies, a major interest is now focused on the evolutionary processes at play rather than the diversity patterns themselves (23). Four alternative evolutionary trajectories of diversity dynamics could be hypothesized to explain the Neotropical diversity observed today: …”.

    However, we will argue as well that some contemporary studies still rely on the cradle and museum framework to frame their studies, for example: McKenna et al. (2006 - PNAS), Couvreur et al. (2011 - BMC Biol.), Condamine et al. 2012 (BMC Evol. Biol.), Moreau & Bell (2013 - Evolution), Dornburg et al. (2017 - Nat. Ecol. Evol.). A search in Google Scholar with "Neotropic* AND cradle* AND diversif*" returns 1,700 results since 2010. That is why we would like to emphasize that this framework should be abandoned, because it does not rely on evolutionary processes and does not consider the full spectrum of hypotheses explaining Neotropical diversity. In the revised version, we have qualified our assertion that most studies are based on these models, which we agree is not entirely true. We have modified the corresponding paragraph as follows: “Attempts to explain Neotropical diversity traditionally relied on two evolutionary models. In the first, tropical regions are described as a “cradle of diversity”, [...] Although not mutually exclusive (15), the cradle vs. museum hypotheses primarily assume evolutionary scenarios in which diversity expands through time without limits (16). However, expanding diversity models may be limited in their ability to explain the entirety of the diversification phenomenon in the Neotropics. For example, expanding diversity models cannot explain the occurrence of ancient and species-poor lineages in the Neotropics (17–19) or the decline of diversity observed in the Neotropical fossil record (20–22). Although the concepts of cradle and museum have contributed to stimulate many macroevolutionary studies, the major interest is now focused on the evolutionary processes at play rather than the diversity pattern (23)”. We hope you will find this new paragraph better represents current thinking in the field.

    There are potentially interesting differences in the diversification dynamics of plants and animals, but this depends on whether we can believe the inferences of the diversification dynamics or not.

    Thank you for pointing this out. We understand the concern because of the general (not new) skepticism on macroevolutionary models (e.g. Kubo & Iwasa 1995 - Evolution; Rabosky & Lovette 2008 - Evolution; Burin et al. 2019 - Syst. Biol.; Louca & Pennell 2020 - Nature; Pannetier et al. 2021 - Evolution). Unfortunately, the study of PDR did not help to confirm/reject this particular conclusion.

    We thus remain cautious with our results, and we have acknowledged several caveats that should be kept in mind when interpreting them. Here, the same methodological treatment has been applied to both animals and plants, and yet the results indeed indicate different diversification patterns. In addition, our results remained stable to AIC variations (Figure 5 - figure supplement 1), and regardless of the paleo-temperature curve considered for the analyses. Still, we do not “believe” the inferences made with birth-death models in general are accurate, but as long as these models are applied in a well-defined framework and thoroughly performed with a hypothesis-driven approach, recent studies have shown that one can interpret the results and draw conclusions (Helmstetter et al. 2021 - Syst. Biol.; Morlon et al. 2022 - TREE).

    For this new version of the manuscript, and following the suggestions of reviewer 3, we have conducted new analyses to assess whether the contrasted diversification dynamics found here between plants and tetrapods could be explained by differences in their datasets (i.e. differences in tree size, crown age, or sampling fraction of the phylogenies). We found that the higher proportion of increasing dynamics observed in plants cannot be explained by significant differences in these factors, strengthening our conclusions.

    Reviewer #2 (Public Review):

    In this study, the authors explored the evolution dynamics of Neotropical biodiversity by analyzing a very large data set, 150 phylogenies of seed plants and tetrapods. Furthermore, they compared diversification models with environment-dependent diversification models to seek potential drivers. Lastly, they evaluated the evolutionary scenarios across biogeographic regions and taxonomic groups. They found that most of the clades were supported by the expansion model and fewer were supported by saturation and declining models. The diversity dynamics do not differ across regions but differ substantially across taxa. The data set they compared is impressive and comprehensive, and the analysis is rigorous. The results broadened our understanding of the evolutionary history of the Neotropical biodiversity which is the richest in the world. It will attract broad interest to evolutionary biologists as well as the public interested in biodiversity.

    Thank you very much for your review and the positive input.

    Reviewer #3 (Public Review):

    This manuscript seeks to address a series of questions about lineage diversification in the Neotropics. The authors first fit a range of lineage diversification models to over 150 neotropical seed plant and tetrapod phylogenies to characterize diversification dynamics. Their work indicates that a constant diversification model was most frequently the best fit model, while time-, temperature- and Andean uplift-dependent models were far less frequently favored. The authors then attempted to determine whether distinct biogeographic clusters existed by using clade abundance patterns as a proxy for long-term diversification within regions. They found that while clades were widespread across ecoregions, regional assemblages could be binned into five clusters reflecting clade endemism. Finally, they asked whether diversification dynamics of individual lineages varied by parent clade, by environment (temperature through time, and Andean uplift) and by biogeographic region, finding that diversity trajectories best explained by environmental drivers and parent clade identity, while no significant association was detected with biogeographic region. I especially appreciated the detailed model-testing procedure, the inclusion of pulled rates, tests for phylogenetic signal in the results, and the acknowledgment of caveats. By using a massive dataset and, and a battery of cutting-edge analyses, the authors provide new insight into questions that have intrigued biologists for decades.

    Thank you for reviewing our study and for your positive feedback.

    1. The neotropics, as defined here, extends from Tierra del Fuego to Central Florida, rather than from the Tropic of Cancer-Capricorn. I was confused by this broad circumscription, and wondered whether the findings presented here could be biased by the inclusion of these exclusively or primarily extra-tropical regions (such as "elsewhere" and "Chaco+Temperate south America") and lineages.

    Thank you for this comment, which is also in line with the second comment of Reviewer 1. We understand the confusion. The Neotropics, as originally defined by Alfred Wallace, represent a broad region including many types of ecosystems and biomes (not only tropical ones): i.e. the Neotropical realm. It also has a paleobiogeographic significance, as the whole South American continent was isolated for tens of millions of years (Simpson 1983). This definition is well accepted in the field of biogeography and evolutionary biology and we followed it to avoid adding a new definition. A Google Scholar search with keywords “Neotropic* AND phylogen* AND diversificat*” returns >24,000 hits. Our biogeo-regionalization and clustering results also corroborate the strong connection between South American temperate and tropical biotas: very few clades were restricted or exclusive to a single region, and in most cases, clades comprised species from tropical regions (Cerrado, Caatinga) together with species from the temperate South America zones (Chaco, Temperate South America; Figure 6, Source Data 1).

    That being said, we did not find significant differences in diversification rates (or diversity dynamics) across temperate and tropical regions (indeed, between any region), even if temperate regions were analyzed separately (Figure-6-figure supplement 2), suggesting that our results would have been similar if we had confined the Neotropics to tropical latitudes, as in a more climatic circumscription. Although, if we would have circumscribed the Neotropics to the tropical latitudes, many of the 150 clades would have not been selected. Hence, our study would have less insights into our understanding of the diversification processes explaining the Neotropical biodiversity in the broad sense.

    1. Model categories and clade diversification dynamics were also linked to the size and age of the phylogeny, such that small and young clades tended to exhibit constant diversification, while exponential and declining dynamics were linked to more diverse and older clades. As one of the main conclusions is that seed plant diversification is more frequently characterized by constant diversification (relative to that of tetrapods), I cannot help but wonder if seed plant phylogenies tend to also be younger and less diverse than those of tetrapods. Figure S1 shows distributions an overview of the distribution but lacks a formal, statistical comparison.

    This is a very good point. We agree this comparison is relevant to support our conclusions, but it was missing from our results. We have now compared tree size, crown age and sampling fraction across taxonomic groups, and found that the higher proportion of increasing dynamics, characteristic of plants, cannot be explained by significant differences in these factors. As can be seen in new Figure-2-figure supplement 2 on the manuscript, tree size does not differ among plants, mammals, birds and squamates. Crown age does not differ among plants, mammals and birds. Groups do differ on sampling fraction: plant (p < 0.01) and squamate (p < 0) phylogenies are significantly worst sampled than the phylogenies of other groups. Yet plants show a higher frequency of increasing dynamics than squamates, and other tetrapods (Figure 4). Incomplete taxon sampling has the effect of flattening out lineages-through-time plots towards the present, and thus artificially increasing the detection of diversification slowdowns rather than diversification increases (Cusimano & Renner 2010 – Syst. Biol.).

    We have included this important piece of information in the results “In our dataset, amphibian phylogenies are significantly larger than those of other clades (p < 0.05) (Figure 2 - figure supplement 2). Amphibian and squamate phylogenies are also significantly older (p < 0). Groups also differ in sampling fraction: plant (p < 0.01) and squamate (p < 0) phylogenies are significantly worst sampled than phylogenies of other groups.”; and in the discussion section: “Differences in the phylogenetic composition of the plant and tetrapod datasets do not explain this contrasted pattern. On average, plant phylogenies are not significantly younger or species-poorer than tetrapod phylogenies (Figure 2 - figure supplement 2). Yet, the proportion of clades experiencing increasing dynamics is significantly higher for plants (Figure 4). Plant phylogenies are significantly worst sampled than those of most other tetrapods, though, as explained above, incomplete taxon sampling has the opposite effect: flattening out lineages-through-time plots towards the present (83).”

    1. I wondered whether it was possible to disentangle time-dependent decreasing diversification from decreasing temperature in young trees? I raise this because it appears that (generally speaking) most of the clades have diversified over periods in which temperature has generally been declining.

    This is also a very good point. It is common to observe that two different models are equally likely or close in terms of statistical support. Previously, Condamine et al. (2019 - Ecol. Lett.) reported that the ΔAIC between the best and second-best diversification model was often below the threshold of 2, which is typically chosen to statistically distinguish models (see Fig. 3 and Fig. S5 in Condamine et al. 2019). Simulation analyses confirmed that it was not enough to distinguish the best and second-best models with confidence (see Fig. S6 in Condamine et al. 2019). This applies to any kind of clade.

    However, in the case of time-dependent decreasing diversification and temperature-dependent decreasing diversification, one can further test the effect of past temperatures by smoothing more the temperature curve so that the features of ups and downs are removed. Previously, Condamine et al. (2019 - Ecol. Lett.) found that smoothing strongly decreased the support for temperature-dependent models (Fig. S13a) to the point where it was lost (Fig. S13b), showing that the support for temperature-dependent models was not simply due to a temporal trend in diversification rates potentially unlinked to temperature.

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  2. Evaluation Summary:

    This paper analyzes data from 150 previously published phylogenies of plants and animals from the Neotropics. A range of diversification models is fit in order to characterize patterns of diversification through time and across space. The authors reveal five biogeographic provinces within which long-term diversification has occurred, but they find that contrasting patterns of diversification for lineages are better explained by their phylogenetic relationship than by biogeographic province, such that the observed modern diversity of seed plants and tetrapods is a consequence of the groups' contrasting diversification dynamics. This paper is of potential interest to a broad audience of biologists who are working on the evolution of large-scale biodiversity, diversity hotspots, lineage diversification, and biogeography.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)

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  3. Reviewer #1 (Public Review):

    This paper address the "origins and drivers of Neotropical diversity." The Neotropics have high diversity of plants and animals relative to other global regions. There are also many hotspots of global biodiversity (species richness) within the Neotropics.

    This paper aggregates 150 time-calibrated phylogenies from different groups of plants and animals that occur predominantly in the Neotropics. They analyze the diversification dynamics of these clades over time primarily using the method of Morlon et al. (2011; PNAS) as implemented in RPANDA (Morlon et al. 2016). The authors find that most clades have constant rates of speciation and extinction over time.

    The strength of the paper is that it aggregates many previously published phylogenies of Neotropical organisms. However, it is unclear whether the method used gives meaningful inferences about diversification dynamics over time (e.g. Burin et al. 2019; Syst. Biol.). Therefore, the overall contribution of the study is somewhat questionable.

    The design of the study is also somewhat problematic. There is no comparison to other regions outside the Neotropics, so the study cannot address why the Neotropics are so diverse relative to other continental regions. Similarly, within the Neotropics, the authors do not find significant differences in diversification rates or dynamics among regions. As far as I can tell, they do not attempt to relate patterns of diversification to patterns of species richness among regions within the Neotropics (and presumably they would find no significant patterns if they did).

    The authors set up their study by claiming that most previous attempts to explain Neotropical diversity relied on two evolutionary models: cradles vs. museums of diversity. The justification cited for this thinking comes mostly from papers from the last century or before. I do not think that this represents the cutting edge of modern thinking about this topic. Many researchers moved on from this dichotomy long ago.

    There are potentially interesting differences in the diversification dynamics of plants and animals, but this depends on whether we can believe the inferences of the diversification dynamics or not.

    Was this evaluation helpful?
  4. Reviewer #2 (Public Review):

    In this study, the authors explored the evolution dynamics of Neotropical biodiversity by analyzing a very large data set, 150 phylogenies of seed plants and tetrapods. Furthermore, they compared diversification models with environment-dependent diversification models to seek potential drivers. Lastly, they evaluated the evolutionary scenarios across biogeographic regions and taxonomic groups. They found that most of the clades were supported by the expansion model and fewer were supported by saturation and declining models. The diversity dynamics do not differ across regions but differ substantially across taxa. The data set they compared is impressive and comprehensive, and the analysis is rigorous. The results broadened our understanding of the evolutionary history of the Neotropical biodiversity which is the richest in the world. It will attract broad interest to evolutionary biologists as well as the public interested in biodiversity.

    Was this evaluation helpful?
  5. Reviewer #3 (Public Review):

    This manuscript seeks to address a series of questions about lineage diversification in the Neotropics. The authors first fit a range of lineage diversification models to over 150 neotropical seed plant and tetrapod phylogenies to characterize diversification dynamics. Their work indicates that a constant diversification model was most frequently the best fit model, while time-, temperature- and Andean uplift-dependent models were far less frequently favored. The authors then attempted to determine whether distinct biogeographic clusters existed by using clade abundance patterns as a proxy for long-term diversification within regions. They found that while clades were widespread across ecoregions, regional assemblages could be binned into five clusters reflecting clade endemism. Finally, they asked whether diversification dynamics of individual lineages varied by parent clade, by environment (temperature through time, and Andean uplift) and by biogeographic region, finding that diversity trajectories best explained by environmental drivers and parent clade identity, while no significant association was detected with biogeographic region. I especially appreciated the detailed model-testing procedure, the inclusion of pulled rates, tests for phylogenetic signal in the results, and the acknowledgment of caveats. By using a massive dataset and, and a battery of cutting-edge analyses, the authors provide new insight into questions that have intrigued biologists for decades.

    1. The neotropics, as defined here, extends from Tierra del Fuego to Central Florida, rather than from the Tropic of Cancer-Capricorn. I was confused by this broad circumscription, and wondered whether the findings presented here could be biased by the inclusion of these exclusively or primarily extra-tropical regions (such as "elsewhere" and "Chaco+Temperate south America") and lineages.

    2. Model categories and clade diversification dynamics were also linked to the size and age of the phylogeny, such that small and young clades tended to exhibit constant diversification, while exponential and declining dynamics were linked to more diverse and older clades. As one of the main conclusions is that seed plant diversification is more frequently characterized by constant diversification (relative to that of tetrapods), I cannot help but wonder if seed plant phylogenies tend to also be younger and less diverse than those of tetrapods. Figure S1 shows distributions an overview of the distribution but lacks a formal, statistical comparison.

    3. I wondered whether it was possible to disentangle time-dependent decreasing diversification from decreasing temperature in young trees? I raise this because it appears that (generally speaking) most of the clades have diversified over periods in which temperature has generally been declining.

    Was this evaluation helpful?