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\begin{document}

\title{The origin and drivers of Neotropical plant and tetrapod diversification}



\author[1]{Andrea Meseguer}%
\author[2]{Alice Michel}%
\author[3]{Pierre-Henri Fabre}%
\author[4]{Oscar Perez Escobar}%
\author[5]{Guillaume Chomicki}%
\author[6]{Ricarda Riina}%
\author[4]{Alexandre Antonelli}%
\author[7]{Carlos Jaramillo}%
\author[8]{Pierre Olivier Antoine}%
\author[2]{Frederic Delsuc}%
\author[9]{Fabien Condamine}%
\affil[1]{INRA}%
\affil[2]{Centre National de la Recherche Scientifique}%
\affil[3]{Universite de Montpellier}%
\affil[4]{Royal Botanic Gardens Kew}%
\affil[5]{University of Oxford}%
\affil[6]{Real Jardín Botánico de Madrid CSIC}%
\affil[7]{STRI}%
\affil[8]{University of Montpellier}%
\affil[9]{CNRS}%


\vspace{-1em}



  
  \date{May 24, 2024}


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\selectlanguage{english}
\begin{abstract}
The assembly of the world's most biodiverse region, the Neotropics, was
traditionally considered the result of long-term environmental
stability. Studies gathered during the last decades suggest that
environmental ``instability'' instead, specially the dramatic
modifications caused by the uplift of the Andes, was responsible of the
Neotropical diversity. Yet a comprehensive understanding has been
hindered by a lack of large-scale comparative data across wide
phylogenetic and ecological contexts. Here, we evaluate the timing and
drivers of Neotropical diversification in a large sample of Neotropical
clades: 150 phylogenies (12,524 species) of seed plants and major
tetrapods (amphibians, mammals, squamates, and birds). We unveil five
trends: (1) biodiversity levels before the Quaternary were comparable
(or higher) to those of the present,; (2) half of the clades diversified
at constant rates; (3) past environmental variations correlate with
diversification changes in 37\% of the lineages, but with contrasting
responses: (4) birds and mammals diversified extensively during warm
periods and global cooling resulted in synchronized slowdowns of
diversification; plant diversification generally increased during
cooling; and (5) the rise of the Andes mostly impacted amphibians and
squamates. Our study suggests that environmental instability over
macroevolutionary scales may in fact act as a driving force of
Neotropical diversification.%
\end{abstract}%



\sloppy


\textbf{Introduction}

Comprising South America, Central America, tropical Mexico and the
Caribbean Islands, the Neotropics are arguably the most biodiverse
region on Earth. This region not only includes the largest tropical
rainforest, Amazonia, but also eight of the 34 known biodiversity
hotspots (Mittermeier \emph{et al.} 2011). The tropical Andes, in
particular, is considered the most species-rich biome in the world for
amphibians, birds, and plants, Mesoamerica and the Caribbean Islands are
the richest regions for squamates, while Amazonia is seen as the primary
biogeographic source of Neotropical biodiversity (Antonelli \emph{et
al.} 2018c). The age and underlying causes of the extraordinary
Neotropical biodiversity represent one of the most debated topics in
evolutionary ecology (Haffer 1969; Simpson 1980; Gentry 1982), but the
mechanisms behind its origin and maintenance remain elusive (Leigh
Jr\emph{et al.} 2004; Hoorn \emph{et al.} 2010; Antonelli \& Sanmart\selectlanguage{ngerman}ín
2011; Rull 2011a).

A long-held tenet was that the outstanding levels of Neotropical
diversity were mainly generated during the Quaternary (\emph{i.e.} the
past 2.6 million years {[}Myrs{]}), as the product of recent
environmental fluctuations (Haffer 1969; Rull 2011a). However, this
hypothesis was challenged by the age of the most recent common ancestors
(MRCA) of Neotropical taxa (Hoorn \emph{et al.} 2010) and fossil studies
showing a fossil record significantly more diverse in the Eocene than
posteriorly (Jaramillo \emph{et al.} 2006). Although recent studies show
that modern climate (Moritz \emph{et al.} 2000; Rull 2011a;
Rowan\emph{et al.} 2019) and intrinsic biological traits (Smith \emph{et
al.}2014) could have contributed to explain the maintenance of
Neotropical diversity during the last few million years, megadiversity
levels in the Neotropics probably existed before the Quaternary. Under
this understanding, short temporal scales might be limited to study this
pattern and historical eco-evolutionary factors need be investigated to
understand the origin and evolution of the Neotropical diversity.

For a long time, the long-term stability and large extension of the
tropical biome across the South American continent and tens of million
years of continental isolation have been argued as the main factors
promoting the gradual accumulation of lineages in the Neotropics
(Wallace 1878; Stebbins 1974; Simpson 1980). Yet, new studies gathered
during the last decade suggest instead that long-term environmental
instability -- geological and environmental perturbations together with
intermittent land connections, mostly during the Neogene -- have been
responsible for the outstanding Neotropical diversity
(Mittelbach\emph{et al.} 2007; Hoorn \emph{et al.} 2010; Rull 2011a;
Antonelli\emph{et al.} 2018b).

Among all potential environmental perturbations, the orogenesis of the
Andes and associated geomorphological and ecological modifications has
become paradigmatic for explaining Neotropical biodiversity (Gentry
1982; Hughes \& Eastwood 2006; Hoorn \emph{et al.} 2010; Luebert \&
Weigend 2014; Antonelli \emph{et al.} 2018a; Esquerré \emph{et
al.}2019). Andean uplift began in the Central Andes \textasciitilde{}65
Myrs ago (Mya) as a result of subduction of the Nazca plate along the
Pacific margin, and in the Northern Andes \textasciitilde{}23 Mya, with
the collision of the Pacific plate. Uplift then intensified
\textasciitilde{}12-4.5 Mya (Garzione \emph{et al.} 2008; Hoorn \emph{et
al.} 2010; Chen \emph{et al.} 2019). The Andean orogeny deeply affected
regional climate, hydrological conditions and landscape evolution at a
continental level, with increased eastern rainfall and sediment flux
into Amazonia (Hoorn \emph{et al.} 1995; Armijo \emph{et al.} 2015).
This process resulted in the modern configuration of the Amazon drainage
basin and fluvial system less than 10 Mya, and contributed to the
formation of the ``dry diagonal'' Caatinga-Cerrado belt
(Blisniuk\emph{et al.} 2005; Hoorn \emph{et al.} 2010, 2017). This
tectonic rearrangement also led to the closure of the Central American
Seaway \textasciitilde{}10 Mya (Jaramillo 2018).

The dynamic landscape caused by the Andean uplift has been postulated to
have a major effect on Neotropical diversification by
\emph{(i)}increasing habitat and environmental heterogeneity (today all
major biomes appear in the region, \emph{e.g.} tropical forests,
deserts, and high elevation grasslands), \emph{(ii)} favoring isolation
and thus allopatric speciation in montane populations separated by deep
valleys, lowland populations on either side of the emerging mountains,
and Amazonian populations separated by new riverine barriers
(Flantua\emph{et al.} 2019), and by \emph{(iii)} creating the longest
latitudinally-elongated corridor for biotic montane dispersal
(Antonelli\emph{et al.} 2009; Luebert \& Weigend 2014). As such, Andean
uplift has been associated with the explosive radiation of plants,
insects, and tetrapods (Weir 2006; Drummond \emph{et al.} 2012;
Lagomarsino \emph{et al.} 2016; Pérez-Escobar \emph{et al.} 2017;
Pouchon \emph{et al.} 2018; Chazot \emph{et al.} 2019; Esquerré \emph{et
al.} 2019), and with increased rates of biotic interchange (Santos
\emph{et al.} 2009; Fjeldså \emph{et al.} 2012; Antonelli \emph{et al.}
2018c; Bacon\emph{et al.} 2018).

Analyses of the fossil record also suggest that Neotropical diversity
has been strongly linked to temperature (Hoorn \emph{et al.} 1995;
Jaramillo \emph{et al.} 2006). Global temperatures were warmer during
the Cretaceous and early Paleogene, a period punctuated with
hyperthermal events, such as the Paleocene-Eocene Thermal Maximum (PETM)
\textasciitilde{}56 Mya. The late Paleogene marks the onset of a
long-term cooling trend that was accelerated at the beginning of the
Quaternary leading to the glaciation-interglaciation climate of the past
2.6 Myrs (Zachos \emph{et al.} 2008; Veizer \& Prokoph 2015). In South
America, global cooling promoted the expansion of open habitats and the
subsequent establishment of fire regimes in the Cerrado savannas
(Simon\emph{et al.} 2009; Antoine \emph{et al.} 2013). These past
climatic events are also thought to have shaped Neotropical
diversification (Pinto\selectlanguage{english}-Ledezma \emph{et al.} 2017). Plant diversity
inferred from fossil morphotypes increased with warming periods during
the Eocene, and decreased sharply with subsequent cooling (Hoorn
\emph{et al.} 1995; Jaramillo \emph{et al.} 2006). Quaternary glacial
cycles have been considered to promote fragmentation in rainforest
ecosystems and high-altitude habitats (\emph{e.g.} through altitudinal
shifts in Andean vegetation zones), which in turn contributed to
geographical isolation and diversification (Haffer 1969; Rull 2011a;
Flantua \emph{et al.}2019). Diversification of Neotropical clades have
also been attributed to more ancient climatic events, such as the PETM
and the cooling event subsequent to the Middle-Miocene climatic optimum
(MMCO) (Hughes \& Eastwood 2006; Lagomarsino \emph{et al.} 2016).

These alternative but non-exclusive models of diversification in the
Neotropics have been difficult to tease apart empirically for two
reasons. Firstly, there has been a lack of large-scale comparative data
across wide phylogenetic and ecological contexts. Secondly, it has been
challenging to develop environmentally explicit diversification models
linking changes in the physical environment and species diversification
(Condamine \emph{et al.} 2013, 2019). Some studies have focused on
particular Neotropical clades to infer their triggers of diversification
(Lagomarsino \emph{et al.} 2016; Esquerre \emph{et al.} 2019), but given
the vast heterogeneity of the region, general insights can only be
provided if patterns of diversification are shared among Neotropical
lineages. Here, we use a comparative phylogenetic data set containing
150 well-sampled species-level molecular phylogenies and 12,524 species.
Our data set represents \textasciitilde{}60\% of all estimated tetrapods
and \textasciitilde{}7\% of the known plant Neotropical diversity, which
we use to evaluate the timing and drivers of Neotropical diversification
at a continental scale. Our results reveal an ancient pre-Quaternary
origin of Neotropical diversity, as well as striking effects of climatic
and landscape changes on Neotropical diversification, with varying
degrees of importance and effect depending on organismal biology and
identity.

\textbf{Results}

Neotropical Phylogenetic Dataset. We constructed a dataset of 150
time-calibrated clades of Neotropical tetrapods and plants derived from
densely sampled molecular phylogenies (\textbf{Fig. 1} and \emph{SI
Appendix 1} and Fig. S1). The dataset comprises 12,524 species divided
into 6,255 species of plants, including gymnosperms and angiosperms (66
clades, representing 7\% of the described Neotropical seed plants;
\emph{SI Appendix} , Table S1); 900 mammal species (12 clades, 75\% of
the Neotropical mammals; \emph{SI Appendix} , Table S2); 2,216 bird
species (32 clades, 59\% of the Neotropical birds; \emph{SI Appendix} ,
Table S3); 1,148 squamate species (24 clades, 33\% of the Neotropical
squamates; \emph{SI Appendix} , Table S4); and 2,005 amphibian species
(16 clades, 69\% of the Neotropical amphibian diversity; \emph{SI}
\emph{Appendix} , Table S5). Our dataset triplicates the data presented
in previous meta-analyses of the Neotropics in terms of number of
species (214 clades and 4450 species in ref. (Antonelli\emph{et al.}
2018c), and quadruplicates it in terms of sampling (20.8 species per
tree in ref. (Antonelli \emph{et al.} 2018c) \emph{vs} . 83.5 in our
study). Each clade in our dataset included 7 to 789 species (mean = 83.5
species), with 53\% of the phylogenies including more than 50\% of the
described taxonomic diversity (sampling mean = 57\%; \textbf{Fig. 1} and
\emph{SI Appendix} , Fig. S1). Clade ages of current Neotropical
diversity range from 0.9 to 88.5 Myrs (mean = 30.4 Myrs), with the
origin of current squamates (mean = 47.5 Myrs) and amphibians (mean = 66
Myrs) being comparatively older than the age of other groups
(mean\textsubscript{birds} = 18.1 Myrs, mean\textsubscript{mammals} =
25.6, mean\textsubscript{plants} = 22.5 Myrs; \textbf{Fig. 1}
and\emph{SI Appendix} , Fig. S1).

Diversification Dynamics in the Neotropics. To understand the drivers of
Neotropical diversification we compared the fit of birth-death models
applied to 150 phylogenies, including models where diversification rates
are constant, vary through time, vary as a function of past global
temperatures, or vary according to past Andean elevation (see
\emph{Methods} ). Models assuming constant speciation and extinction
rates through time best fit half of the phylogenies in our study (75
clades; 2,903 species; \textbf{Fig. 2} and \emph{SI Appendix 2} and
Table S6 and Fig. S2), often when clades are species-poor
(Kruskal-Wallis chi-squared test: \selectlanguage{greek}\emph{χ\textsuperscript{2}}\selectlanguage{english} = 53.675,
df = 3, \emph{P} = 0.0; \emph{SI Appendix} , Table S7 and Fig. S2).
Phylogenies best fitting a constant model are also significantly younger
than those fitting Andean uplift and temperature models
(\selectlanguage{greek}\emph{χ\textsuperscript{2}}\selectlanguage{english} = 41.96, df = 3, \emph{P} = 0.0), even
though young clades do not tend to be species-poor (\emph{SI Appendix} ,
Fig. S3). Taxon sampling does not differ significantly between the four
model categories investigated here, suggesting that there is not a
particular bias due to incomplete sampling in our results
(\selectlanguage{greek}\emph{χ\textsuperscript{2}}\selectlanguage{english} = 4.01, df = 3, \emph{P} = 0.26; \emph{SI
Appendix} , Table S7 and Fig. S2).

In the other half of the phylogenies analyzed here, representing most of
the Neotropical diversity (75 trees; 9,621 species; \textbf{Fig. 3}
and\emph{SI Appendix} , Table S8), we find variation in diversification
rates through time, with 42 clades (4,486 species) showing slowdowns of
diversification and 33 increasing diversification (5,135 species). Rate
variation is inferred from models that are able to capture the
dependency of speciation and/or extinction rates over time
(time-dependent models) or over an environmental variable (either
temperature- or uplift-dependent models). Temperature-dependent models
explain diversification in 26\% of the phylogenies and 44\% of the
species sampled (5,487 species). Time-dependent models best fit 13\% of
the clades (1,717 species, 13\%). Meanwhile uplift-dependent models
explain 11\% of the phylogenies (2,417 species, 19\%) (\textbf{Fig.
2}and \emph{SI} \emph{Appendix} , Table S9), especially for ancient
clades (\selectlanguage{greek}\emph{χ\textsuperscript{2}}\selectlanguage{english} = 53.675, df = 3, \emph{P} = 0.0;
\emph{SI Appendix} , Table S7 and Fig. S2). Seven of these clades have
an Amazonean-centered distribution and are better fit by an uplift
model.

We did not detect significant differences in diversification trends
(\emph{i.e.,} increasing, constant, decreasing) estimated between
tetrapod lineages living in distinct geographic ranges (Andean-centered,
Amazonian-centered, or other), elevations (lowland {[}\textless{}1000
m{]}, montane {[}1000 -- 3000 m{]}, or highland {[}\textgreater{}3000
m{]}) or vegetation types (open tropical vegetation, tropical forest, or
non-tropical vegetation). For plants, we perceived, however, a
marginally non-significant difference in the frequency of
Amazonian-centered clades showing decreasing diversification through
time in comparison with Andean-centered and lineages with other
distribution (\selectlanguage{greek}\emph{χ\textsuperscript{2}}\selectlanguage{english} = 5.69, df = 2, \emph{P} =
0.058).

\textbf{Discussion}

The Origin of Neotropical Biodiversity. All evidence generated in our
analyses suggests that Neotropical biodiversity attained outstandingly
high levels prior to the Quaternary. The age of the MRCA of most clades
analyzed here (146 clades out of 150, 97\%) largely predates the
Quaternary (\textbf{Fig. 1} ; mean age of 30.4 Myrs), supporting the
results of (Hoorn \emph{et al.} 2010). The MRCA of clades and genera,
however, do not inform on the diversification of their descendant
species (Rull 2011b). This is instead informed by the diversification
rates calculated here, which for most Neotropical lineages have remained
constant through time (75 clades, 50\%; 2903 species, 23\%) or were
higher in the past and diversification decreased toward the present (42
clades, 28\%; 4486 species, 36\%) (\textbf{Fig. 3} ). This result
suggests that the total number of species in the Neotropics was probably
as high (or higher) before the Quaternary than today, a result
previously only reported from the fossil record (Jaramillo \emph{et al.}
2006; Salas-Gismondi \emph{et al.} 2015).

Diversification Drivers for Tetrapods. A substantial number of
Neotropical tetrapod clades studied here (44\%) evolved under a constant
rate during the Cenozoic (\textbf{Fig. 2} ), although this proportion is
smaller when the number of species is accounted for (1,204 species,
19\%). Phylogenies best fitting constant models in our study tend to be
smaller and younger than phylogenies fitting other models, and as so, we
find a higher proportion of bird and mammal clades' diversification
dynamics (\textgreater{}50\%) explained by constant-rate models than
amphibian and squamates clades (\textless{}30\%,\textbf{Fig. 1} and
\emph{SI Appendix} , Table S7 and Fig. S2). This could be partly
explained by the observed differences in clade ages between these
groups, with younger clades having, arguably, less time to being exposed
to geological and environmental changes during their history (Smith
\emph{et al.} 2014), but also by our reduced power to detect rate
variation as the number of species decreases (Davis \emph{et al.} 2013).
The remaining tetrapod diversification is generally best explained by
speciation rates decreasing through time and extinction remaining
constant (\textbf{Fig. 3} and \emph{SI Appendix} , Table S9), a pattern
that is especially manifest in endotherms, and among them in birds.
Regardless of their ecology or distribution, all bird clades exhibit
diversification slowdowns (\textbf{Fig. 3} and \emph{SI Appendix} ,
Tables S3 and S9).

The pattern of decreasing diversification in Neotropical endotherms is
consistent with previous studies suggesting a general trend for
slowdowns in speciation at continental scales and across taxonomic
groups (McPeek 2008; Phillimore \& Price 2008; Morlon \emph{et al.}2010;
Luzuriaga-Aveiga \& Weir 2019), which has been often interpreted as the
signal of ecological limits on the number of species within a clade
(Rabosky 2009). Among the phylogenies supporting diversification
slowdowns here, time-dependent models explain 8\% of all tetrapod
phylogenies, but the proportion is highest for mammals
(25\%,\textbf{Fig. 2} and \emph{SI Appendix} , Table S10 and Figs S4-5).
Time-dependent models with decreasing speciation have been suggested to
be a good approximation of diversity-dependent diversification
(Rabosky\emph{et al.} 2014). Our results lend support to an alternative
explanation for diversification slowdowns: the idea that clades fail to
keep pace with a changing environment (Moen \& Morlon 2014;
Condamine\emph{et al.} 2019). Our temperature-dependent models explain a
substantial proportion of phylogenies supporting diversification
slowdowns in our study (17\% of mammal and 38\% of birds; \textbf{Fig.
4} and \emph{SI Appendix} , Figs S6-7). The positive correlation between
diversification and past temperature indicates that these groups
diversified more during periods of global warming such as the greenhouse
Eocene or the MMCO, and speciation decreased during colder periods (such
as the Eocene-Oligocene transition and the late Miocene onwards).

Temperatures can influence diversification in different ways. According
to the Metabolic Theory of Biodiversity, high temperatures can increase
enzymatic activity, generation times and mutation rates
(Gillooly\emph{et al.} 2001), which may in turn affect diversification
positively, and conversely (Allen \emph{et al.} 2006; Condamine \emph{et
al.} 2019). Climate cooling could also decrease global productivity,
resource availability, and population sizes (Mayhew \emph{et al.} 2012)
or even species interactions (Jaramillo \& C\selectlanguage{ngerman}árdenas 2013;
Chomicki\emph{et al.} 2019). Reduction of the tropical forest biome
(Jaramillo 2019) could have also contributed to this pattern of
decreasing diversification in association with climate changes, caused
by decreased precipitation in the Neotropics during Cenozoic cooling
(Silva \emph{et al.} 2019). Only one group of endotherms, the New World
monkeys (Platyrrhini), had increased diversification as temperature
dropped. This result could reflect the role of Quaternary events on
primate speciation (Rull 2011a), or could, however, be an artifact of
taxonomy over splitting species in this clade (Springer \emph{et al.}
2012).

Compared with endotherms, ectotherm tetrapods show a mixed
diversification trend (\textbf{Fig. 3} and \emph{SI Appendix} , Table
S8). We find a similar fraction of amphibians decreasing and increasing
diversification rates through time (668 species and 5
phylogenies\emph{vs.} 823 species and 6 phylogenies, respectively). In
squamates, the diversification of most clades has decreased, but for a
non-negligible proportion it increased (679 species and 13
phylogenies\emph{vs.} 353 species and 4 phylogenies). Contrasting with
endotherms and plants (see below), the triggers of rate variations in
ectotherm diversification are mostly associated with the Andean orogeny
(50\% of amphibian clades and 1,166 species; 33\% of squamate clades and
663 species) rather than with global temperature changes or time
(\textbf{Figs. 2, 5} and \emph{SI Appendix} , Figs. S6 and S7 and Tables
S6 and S9). This is in agreement with the dominant view on Neotropical
ectotherm diversification (Santos \emph{et al.} 2009; Hutter \emph{et
al.} 2013, 2017; Esquerré \emph{et al.} 2019).

The Andes host twice the amphibian richness as the entire Amazonian
lowland rain forest, with more endemic frog species than any other
region in the world (Hutter \emph{et al.} 2017). They also comprise the
third most endemic squamate fauna, after the Caribbean Islands and
Madagascar (Mittermeier \emph{et al.} 2011). Interestingly, we find that
diversification in many lineages (\emph{i.e.} , 649 amphibian and 353
squamate species) correlated positively with the Andean uplift, such
that cladogenesis progressively increased with the orogeny
(\textbf{Figs. 2, 5} ). Some of these clades show an Andean-centered
distribution, such as Liolaemidae and Tropiduridae lizards or
Centrolenidae frogs, but others are predominately distributed outside
the Andes such as Leptodactylidae frogs or Hoplocercidae lizards
(\emph{SI Appendix} , Tables S4-5). Sustained diversification in the
context of Andean orogeny into and out of the Andean region could be
explained by increasing thermal and environmental gradients from
equatorial areas to Patagonia or in a west-east gradient, as it has been
suggested to affect Leptodactylidae and other frogs (Fouquet \emph{et
al.} 2014; Moen \& Wiens 2017). Other possible correlates include
changes in elevational distributions of lineages and concomitant shifts
in climatic regimes (Kozak \& Wiens 2010; Hutter \emph{et al.} 2017),
recurrent migrations from (and within) the Andes into other regions, and
allopatric fragmentation (Santos \emph{et al.} 2009; Esquerré \emph{et
al.} 2019). The explosive generation of new land area that occurs with
mountain building could also explain this pattern (Elsen \& Tingley
2015; Antonelli \emph{et al.} 2018b), \emph{e.g.} , each small ravine
down the mountain has a microtopography with a variety of slopes in
multiple directions.

In a significant proportion of ectotherm clades, however, we also
detected that diversification was elevated only during the early stages
of the orogeny and then decreased with progressive uplift
(\emph{i.e.,}negative correlation between diversification and Andean
orogeny for 472 amphibian and 310 squamate species; \textbf{Fig. 5} and
\emph{SI Appendix} , Figs. S6 and S7), in agreement with diversification
slowdowns detected in recent studies (Santos \emph{et al.} 2009). These
include lineages that are diverse in the Andes, such as dendrobatid
frogs, but also non-Andean lineages, such as Odontophrynidae frogs or
Leiosauridae and Xantusiidae lizards, which abound in the Cerrado,
Chaco, temperate South America, and Mesoamerica.

Andean uplift started in the late Eocene with the formation of moderate
elevation uplands (1,000--1,500 m) in a non-continuous belt, and then
accelerated in the late Miocene, with the majority of the Tropical Andes
reaching its modern elevation \textasciitilde{}4.5 Mya (Garzione\emph{et
al.} 2008; Hoorn \emph{et al.} 2010; Chen \emph{et al.} 2019). Initial
Andean uplift might have stimulated diversification in the lowland
transition zone, with new ecological opportunities in tropical-like
habitats formed at moderate elevation and increased rates of
geographical isolation for species with cross-Andean distributions
(Santos \emph{et al.} 2009). Post-Miocene uplifts, however, built a
major ecological and geological barrier for biotic dispersals of many
groups, with strong physiological constraints limiting adaptations to
new upland environments, or dispersal across unsuitable habitats
(Santos\emph{et al.} 2009; Olalla\selectlanguage{english}-Tarraga \emph{et al.} 2011; Hutter
\emph{et al.} 2013; Pie \emph{et al.} 2017). Taken together, these
results suggest that elevation of the Andes impacted ectotherm
diversification at the continental scale.

\emph{Diversification Drivers for Plants}\textbf{.} In contrast to
tetrapods, the diversification of a significant fraction of Neotropical
plants shows an expanding trend toward the present (4,019 species, 64\%;
22 clades, 33\%), either due to increasing speciation, decreasing
extinction, or both (\textbf{Fig. 3} and \emph{SI Appendix} , Table S9).
Another substantial proportion of plants evolved under a constant rate
model (1,699 species, 27\%; 38 phylogenies, 58\%). Only a small
proportion of Neotropical plant diversity experienced slowdowns of
diversification (537 species, 8.6\%; 6 phylogenies, 9\%). Changes in
plant diversification are also mostly associated with paleotemperatures
(16 clades; 24\%) and with time alone (11 clades; 16\%), while the
effect of the Andes is negligible (1 clade, Gesnerioideae)
(\textbf{Figs. 2, 4} and \emph{SI Appendix} , Figs S6 and S7). This
result is surprising given that Andean uplift has often been considered
the main driver behind the radiation of Neotropical plants, especially
in the Paramo, but also in other regions (Hughes \& Eastwood 2006;
Antonelli \emph{et al.} 2009; Drummond \emph{et al.} 2012; Luebert \&
Weigend 2014; Lagomarsino \emph{et al.} 2016; Perez-Escobar \emph{et
al.} 2017; Bacon \emph{et al.} 2018; Pouchon \emph{et al.} 2018).
Lineages including species distributed in the Paramo are not well
represented in this study, but the few included here --
\emph{Lupinus}(Fabaceae), centropogonids (Campanulaceae),
\emph{Pleurothalis} and\emph{Stelis} (Orchidaceae), \emph{Solanum,
Cestrum} , and \emph{Sessea}(Solanaceae) -- do not follow an uplift
model. This result contrasts with a previous study for Cymbidieae
orchids supporting uplift-dependent diversification (Perez-Escobar
\emph{et al.} 2017), while diversification in this clade is best
explained by temperature-dependent models in our study (\emph{SI
Appendix} , Table S9). Results are however not directly comparable as
ref. (Perez-Escobar \emph{et al.} 2017) only evaluated uplift models.
Similarly, centropogonids diversification is best explained by
temperature-dependent models in ref. (Lagomarsino\emph{et al.} 2016),
but by time-dependent models in our study (\emph{SI Appendix} , Table
S9). Time-dependent models are not evaluated in previous studies
(Lagomarsino \emph{et al.} 2016; Perez-Escobar \emph{et al.} 2017),
though these models probably represent more realistic null hypotheses
than constant-rate scenarios, especially when half of the diversity in
our study is found to have changed diversification rates through time
(\textbf{Fig. 2} ).

Among the plant clades increasing diversification rates through time, in
10 phylogenies (15\% of the clades; 2,180 species, 35\%), we found a
negative correlation between diversification and temperature changes,
indicating that these groups diversified more during cold periods and
due to increasing speciation or decreasing extinction (\textbf{Figs. 3,
4} and \emph{SI Appendix} , Figs. S4-6). In the other 11 clades (1251
species, 20\%), diversification increased as a function of time alone
(\emph{SI Appendix} , Table S10), and generally due to decreases of
extinction while speciation remained constant (\emph{SIAppendix} , Table
S9).

Plant phylogenies increasing diversification rates through time mostly
correspond to clades distributed in the Andes, Choco and Central America
-- also termed ``Andean- centered'' groups (Gentry 1982) -- from
lowlands to highlands, such as \emph{Bactris} palms
(Arecaceae),\emph{Fuchsia} (Onagraceae), or Cymbidieae orchids, among
others (\emph{SI Appendix} , Table S9). Many species within
Andean-centered groups were likely able to adapt to the new conditions
that increasingly appeared in the mountain foothills as the Andes
uplifted and global temperatures dropped (Luebert \& Weigend 2014;
Antonelli \emph{et al.}2018b). It has been proposed that the first
Quaternary glaciation could have acted as a major evolutionary
bottleneck, whereby many warm\selectlanguage{english}-adapted lineages succumbed, while those
that survived could have diversified and better cope with subsequent
climatic oscillations (Silva \emph{et al.}2018). Cenozoic climate
cooling could also have created a ``biotic corridor'' for pre-adapted
lineages to montane conditions to increase their range and colonize new
montane environments (Antonelli \emph{et al.} 2009; Perez-Escobar
\emph{et al.} 2017; Meseguer \emph{et al.}2018). Many iconic
high-elevation Andean clades (e.g. \emph{Espeletia} ) had major
radiations within the past 2.5 Myrs (Madrinan \emph{et al.}2013; Pouchon
\emph{et al.} 2018), about 2 Myrs after the Andes had reached their
modern elevation, suggesting that the onset of the Quaternary climate
could have played a much stronger role in increasing speciation rates
than the generation of high topography in itself. In addition, some of
these clades represent textbook examples of ongoing explosive
radiations; \emph{e.g.} centropogonids (Lagomarsino \emph{et al.} 2016),
\emph{Lupinus} (Hughes \& Eastwood 2006; Drummond \emph{et al.} 2012),
and \emph{Inga} (Richardson \emph{et al.} 2001). Their diversification
has been previously associated with biotic drivers, such as species
interactions (Kursar \emph{et al.} 2009), the evolution of key
adaptations (Drummond \emph{et al.} 2012), or pollination syndromes
(Lagomarsino \emph{et al.} 2016). Although we have not explicitly tested
the impact of intrinsic biological traits in the generation of this
diversity, these results add support to the role of climate and biotic
factors as not mutually exclusive drivers of macroevolutionary changes
in the Neotropics, with the rise of the Andes acting mostly indirectly
by providing the necessary conditions for species to expand and
diversify in new climatic regimes.

In contrast, we detected six clades (537 species) that have decreased
diversification, all associated with global cooling
(including\emph{Sideroxylon} {[}Sapotaceae{]}\emph{,
Guatteria}{[}Annonaceae{]}\emph{, Myrcia} {[}Myrtaceae{]}, among
others). These clades are mostly distributed in lowland regions of
Amazonia, the Brazilian and Guiana Shields -- the Amazonian-centered
elements in Gentry's sense (Gentry 1982) (\emph{SI Appendix} , Table
S9). These groups diversified more during warm periods and climate
cooling negatively impacted their diversification, a result consistent
with paleobotanical studies showing a positive correlation between
Neotropical plant paleodiversity and past temperatures
(Jaramillo\emph{et al.} 2006). Slowdowns of diversification were mainly
due to decreases in speciation (\textbf{Fig. 4} and \emph{SI Appendix} ,
Figs. S5 and S6). Such pattern could be explained by decreases in
primary productivity, but also by the expansion of several biomes,
including Paramo, cloud forests, savannas, and dry/xerophytic forest at
the expense of the reduction of the rainforest during the late Neogene
(Jaramillo 2019).

Conclusion. Environmental perturbations have long been recognized as
fundamental for regulating diversity, although progress toward
understanding how has been slow. Here, we demonstrate that
diversification for a significant fraction of Neotropical clades
correlates with deep-time environmental trends, especially with
temperature changes and to a lesser extent with Andean uplift. The
effect of these environmental perturbations extends to the continental
scale, modulating the pace of Neotropical diversification across
organisms and biomes. Yet, the specific mechanisms by which they impact
diversification are clade-dependent and remain to be understood. The
other fraction of Neotropical diversity evolved at constant rates or is
associated with different extrinsic/intrinsic factors.

Our results have implications for discussing the future of biodiversity
in the context of current environmental changes, and on how it might
recover from human-induced extinction. As global change accelerates,
ecosystems will face an increasing rate of perturbations,
\emph{e.g.}temperatures increase, drought or habitat loss, with current
deforestation rates staggering across all Neotropical biomes. If one
quarter of the Neotropical diversity in our study (\textasciitilde{}3000
species) follows a constant diversification mode as in the past, it may
take tens of millions of years for biodiversity to reach its
pre-extinction level. For most of the remaining Neotropical diversity,
but especially tetrapods and Amazonian plants, past climate cooling
triggered coordinated slowdowns of their speciation rates, suggesting
that the pace of diversification in the world insignia of biodiversity,
the Neotropics, has been in deceleration. Whilst this study found that
ancient climate warming triggered increases in diversification on these
lineages, this relationship must not be extended to the present, as the
pace of current environmental changes is the fastest in geological
history and acting in synergy with multiple biotic stressors lacking
past equivalents (Condamine \emph{et al.} 2013).

\textbf{Materials and Methods}

Additional data and methodology are described in \emph{SI Appendix} .

Data Compilation. We extracted Neotropical clades that included at least
80\% of the species distributed in the Neotropics as defined in
(Antonelli \emph{et al.} 2018c). From large-scale phylogenies, we relied
on the time-calibrated phylogenies of frogs and toads (Hutter \emph{et
al.} 2017), salamanders (Pyron \emph{et al.} , 2013; Pyron, 2014),
Squamata (lizards and snakes) (Pyron \& Burbrink 2014), birds (Jetz
\emph{et al.} 2012) (including only species for which genetic data was
available), mammals (Bininda-Emonds \emph{et al.} , 2007; Kuhn \emph{et
al.} , 2011), and plants (Zanne \emph{et al.} 2014). In addition,
phylogenies of particular lineages not represented in the global trees
(or with improved taxon sampling) were obtained from published studies
(\emph{SI Appendix} , Tables S1-5) or reconstructed\emph{de novo} (for
caviomorph rodents, including 199 species, and phyllostomid bats, 170
species; see \emph{SI Appendix} ). However, whenever possible, we
preferred to extract phylogenies from a single dated tree rather than
performing a meta-analysis of individual trees coming from different
sources (\emph{e.g.,} ref. (Hoorn \emph{et al.}2010; Jansson \emph{et
al.} 2013)), such that divergence times would be comparable. In
addition, this procedure allows reducing the bias of focusing on
particular taxonomic levels (\emph{i.e.,} individual studies often focus
on genera) and thus comparing lineages of similar ages (Wiens 2017).
When the most inclusive Neotropical clade was over the family rank, or
for extremely species-rich groups, like the family Solanaceae with more
than 2,700 species, we split the phylogenies into smaller clades
(\emph{e.g.,} tribes) to take into account the heterogeneity of
evolutionary histories likely characterized by different morphologies
and key adaptations.

Diversification Analyses. We designed and applied a series of 10
birth-death diversification models estimating speciation\selectlanguage{greek}\emph{(λ)}\selectlanguage{english} and
extinction \selectlanguage{greek}\emph{(μ)}\selectlanguage{english} rates for each of the 150 phylogenies with the
R-package RPANDA 1.3 (Morlon \emph{et al.} 2016). We first fitted a
constant-rate birth--death model (null model) and a set of three models
in which speciation and/or extinction vary according to time (Morlon
\emph{et al.} 2011): \selectlanguage{greek}\emph{λ(t)}\selectlanguage{english} and \selectlanguage{greek}\emph{μ(t)}\selectlanguage{english} . For time-dependent
models, we measured rate variation for speciation and extinction with
\selectlanguage{greek}\emph{α} \selectlanguage{english}and \selectlanguage{greek}\emph{β} , \selectlanguage{english}respectively: \selectlanguage{greek}\emph{α} \selectlanguage{english}and\selectlanguage{greek}\emph{β}
\selectlanguage{english}\textgreater{} 0 reflect decreasing speciation and extinction toward the
present, respectively, while \selectlanguage{greek}\emph{α} \selectlanguage{english}and \selectlanguage{greek}\emph{β}\selectlanguage{english}\textless{} 0 indicate
the opposite, increasing speciation and extinction toward the present.

We further investigated the effect of environmental changes, here
approximated by mean global temperatures and paleo-elevations of the
Andes (the main factors hypothesized behind the origin of Neotropical
diversity). Temperature variations during the Cenozoic were obtained
from global compilations of deep-sea oxygen isotope
(\selectlanguage{greek}δ\selectlanguage{english}\textsuperscript{18}O) from ref. (Prokoph \emph{et al.} 2008;
Zachos\emph{et al.} 2008), but also on other different paleotemperature
curves, to assess the impact of paleotemperature uncertainty on our
results (\emph{SI Appendix} ). For Andean paleo-elevations we retrieved
a generalized model of the paleoelevation history of the tropical Andes,
compiled from several references (ref. (Lagomarsino \emph{et al.} 2016)
and references therein)). We examined whether speciation and/or
extinction correlate with one of these variables using
paleoenvironment-dependent diversification models (Condamine \emph{et
al.} 2013), which extends time-dependent models to account for potential
dependencies between diversification rates and measured environmental
variables. The elevation of the Andes caused dramatic modifications in
Neotropical landscapes and could have impacted indirectly the
diversification of non-Andean groups. Therefore, we decided to apply
uplift models to all clades in our study, independently on whether their
distribution is centered in the Andes or not. We fitted three models in
which speciation and/or extinction vary continuously with temperature
changes \selectlanguage{greek}\emph{(λ(T)}\selectlanguage{english} and \selectlanguage{greek}\emph{μ(T))}\selectlanguage{english} , and three others with the
elevation of the Andes \selectlanguage{greek}\emph{(λ(A)}\selectlanguage{english} and \selectlanguage{greek}\emph{μ(A))}\selectlanguage{english} . In this
case,\selectlanguage{greek}\emph{λ\textsubscript{0} (μ\textsubscript{0})}\selectlanguage{english} is the expected
speciation (extinction) rate under a temperature of 0\selectlanguage{ngerman}°C (or a
paleoelevation of 0 m for the uplift models). For the groups in which
diversification was temperature- or uplift-dependent, we analyzed
whether the speciation \selectlanguage{greek}\emph{(α)}\selectlanguage{english} and extinction \selectlanguage{greek}\emph{(β)}\selectlanguage{english} dependency
was positive or negative. For temperature models, \selectlanguage{greek}\emph{α} \selectlanguage{english}(\selectlanguage{greek}\emph{β} \selectlanguage{english})
\textgreater{} 0 reflect increasing speciation (extinction) with
increasing temperatures, and conversely. For the uplift models,
\selectlanguage{greek}\emph{α}\selectlanguage{english}(\selectlanguage{greek}\emph{β} \selectlanguage{english}) \textgreater{} 0 reflect increasing speciation
(extinction) with increasing Andean elevations, and conversely. We
accounted for missing species for each clade in the form of sampling
fraction\selectlanguage{greek}\emph{(ρ)}\selectlanguage{english} (Morlon \emph{et al.} 2011) and assessed the strength
of support of the models by computing Akaike information criterion
(AICc), [?]AICc, and Akaike weights (AIC\selectlanguage{greek}ω\selectlanguage{english}) to select the best-fit model.

Finally, we tested the effect of clade age, size and sampling fraction
on the preferred model using Kruskal-Wallis rank sum test and performed
multiple pairwise-comparison between groups with corrections for
multiple testing using Wilcoxon rank sum test. We also evaluate if the
estimated diversification trends (\emph{i.e.} , increasing, constant,
decreasing) differ between lineages characterized by different
geographic distributions, altitudinal ranges and habitat preferences
(see \emph{SI Appendix} ).

Our study focuses on the effects of environmental factors over
diversity, and in this sense we did not directly assess the effect of
biotic factors. Only few models of that type exist, and none explicitly
incorporate species interactions within clades. The most relevant of
such models are diversity-dependent models where the number of extant
species in a clade affects diversification rates (Etienne \emph{et
al.}2012). We did not fit these models for three additional
reasons:\emph{(i)} it is not straightforward to compare
diversity-dependent models with other diversification models on the
basis of AICc (Etienne\emph{et al.} 2016); \emph{(ii)} the sampling
scheme currently implemented in diversity-dependent models assumes that
exactly \emph{n}species are sampled (\emph{n} -sampling), while other
models assume that each species is sampled with a fixed probability
(\selectlanguage{greek}ρ-\selectlanguage{english}sampling), and likelihoods associated to these two sampling schemes
are not directly comparable (Stadler 2009; Lambert 2017); and
\emph{(iii)} previous simulations have shown that these models tend to
over-fit the data when speciation decreases toward the present
regardless the cause of decline (Etienne \emph{et al.} 2016; Condamine
2018). This latter artifact might affect more than 78\% of clades in our
study, since we found most phylogenies are characterized by constant or
decreasing rates through time (\emph{see Results} ). Nonetheless, we
acknowledge that the role of biotic interactions in explaining
Neotropical diversity remains to be tested.

\textbf{Acknowledgments.} We thank all researchers who shared their
published data through databases or to us directly (Drs. Arevalo,
Martins, Fortes Santos, Simon, Lohmann, Mendoza, Swenson, Erkens, van
der Meijden, and Freitas), Dr. Sanmart\selectlanguage{ngerman}ín and Dr. Manzano for invaluable
comments on the manuscript and analyses. This work was funded by an
``\emph{Investissements d'Avenir} '' grant managed by the Agence
Nationale de la Recherche (CEBA, ref. ANR-10-LABX-25-01) and by the ANR
GAARAnti project (ANR-17-CE31-0009). A.A. is supported by the Knut and
Alice Wallenberg Foundation, the Swedish Research Council, the Swedish
Foundation for Strategic Research, and the Royal Botanic Gardens, Kew.

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