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 (Fig. 1 ; mean age of 30.4
Myrs), supporting the results of (Hoorn 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%) (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 et al. 2006; Salas-Gismondi 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 (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 (>50%) explained by constant-rate
models than amphibian and squamates clades (<30%,Fig. 1 and 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 et al. 2014), but also by our reduced power to
detect rate variation as the number of species decreases (Davis et
al. 2013). The remaining tetrapod diversification is generally best
explained by speciation rates decreasing through time and extinction
remaining constant (Fig. 3 and 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 (Fig. 3 and 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 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%,Fig. 2 and 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 (Raboskyet 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; Condamineet 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; Fig.
4 and 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 (Gilloolyet al. 2001), which may in turn affect diversification
positively, and conversely (Allen et al. 2006; Condamine et
al. 2019). Climate cooling could also decrease global productivity,
resource availability, and population sizes (Mayhew et al. 2012)
or even species interactions (Jaramillo & Cárdenas 2013; Chomickiet 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 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 et al. 2012).
Compared with endotherms, ectotherm tetrapods show a mixed
diversification trend (Fig. 3 and SI Appendix , Table
S8). We find a similar fraction of amphibians decreasing and increasing
diversification rates through time (668 species and 5 phylogeniesvs. 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 phylogeniesvs. 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
(Figs. 2, 5 and SI Appendix , Figs. S6 and S7 and Tables
S6 and S9). This is in agreement with the dominant view on Neotropical
ectotherm diversification (Santos et al. 2009; Hutter et
al. 2013, 2017; Esquerré 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 et al. 2017). They also comprise the
third most endemic squamate fauna, after the Caribbean Islands and
Madagascar (Mittermeier et al. 2011). Interestingly, we find that
diversification in many lineages (i.e. , 649 amphibian and 353
squamate species) correlated positively with the Andean uplift, such
that cladogenesis progressively increased with the orogeny
(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
(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 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 et al. 2017),
recurrent migrations from (and within) the Andes into other regions, and
allopatric fragmentation (Santos et al. 2009; Esquerré et
al. 2019). The explosive generation of new land area that occurs with
mountain building could also explain this pattern (Elsen & Tingley
2015; Antonelli et al. 2018b), 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 (i.e.,negative correlation between diversification and Andean orogeny for 472
amphibian and 310 squamate species; Fig. 5 and SI
Appendix , Figs. S6 and S7), in agreement with diversification slowdowns
detected in recent studies (Santos 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 ~4.5 Mya (Garzioneet al. 2008; Hoorn et al. 2010; Chen 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 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 (Santoset al. 2009; Olalla‐Tárraga et al. 2011; Hutter et
al. 2013; Pie et al. 2017). Taken together, these results
suggest that elevation of the Andes impacted ectotherm diversification
at the continental scale.
Diversification Drivers for Plants. 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 (Fig. 3 and 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)
(Figs. 2, 4 and 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 Páramo, but also in other regions (Hughes & Eastwood 2006;
Antonelli et al. 2009; Drummond et al. 2012; Luebert &
Weigend 2014; Lagomarsino et al. 2016; Pérez-Escobar et
al. 2017; Bacon et al. 2018; Pouchon et al. 2018).
Lineages including species distributed in the Páramo are not well
represented in this study, but the few included here – Lupinus(Fabaceae), centropogonids (Campanulaceae), Pleurothalis andStelis (Orchidaceae), Solanum, Cestrum , and Sessea(Solanaceae) – do not follow an uplift model. This result contrasts
with a previous study for Cymbidieae orchids supporting uplift-dependent
diversification (Pérez-Escobar et al. 2017), while
diversification in this clade is best explained by temperature-dependent
models in our study (SI Appendix , Table S9). Results are however
not directly comparable as ref. (Pérez-Escobar et al. 2017) only
evaluated uplift models. Similarly, centropogonids diversification is
best explained by temperature-dependent models in ref. (Lagomarsinoet al. 2016), but by time-dependent models in our study (SI
Appendix , Table S9). Time-dependent models are not evaluated in
previous studies (Lagomarsino et al. 2016; Pérez-Escobar 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 (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 (Figs. 3,
4 and SI Appendix , Figs. S4-6). In the other 11 clades (1251
species, 20%), diversification increased as a function of time alone
(SI Appendix , Table S10), and generally due to decreases of
extinction while speciation remained constant (SIAppendix , Table S9).
Plant phylogenies increasing diversification rates through time mostly
correspond to clades distributed in the Andes, Chocó and Central America
– also termed “Andean- centered” groups (Gentry 1982) – from
lowlands to highlands, such as Bactris palms (Arecaceae),Fuchsia (Onagraceae), or Cymbidieae orchids, among others
(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 et al.2018b). It has been proposed that the first Quaternary glaciation could
have acted as a major evolutionary bottleneck, whereby many warm‐adapted
lineages succumbed, while those that survived could have diversified and
better cope with subsequent climatic oscillations (Silva 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 et
al. 2009; Pérez-Escobar et al. 2017; Meseguer et al.2018). Many iconic high-elevation Andean clades (e.g. Espeletia )
had major radiations within the past 2.5 Myrs (Madriñán et al.2013; Pouchon 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; e.g. centropogonids (Lagomarsino et
al. 2016), Lupinus (Hughes & Eastwood 2006; Drummond et
al. 2012), and Inga (Richardson et al. 2001). Their
diversification has been previously associated with biotic drivers, such
as species interactions (Kursar et al. 2009), the evolution of
key adaptations (Drummond et al. 2012), or pollination syndromes
(Lagomarsino 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 (includingSideroxylon [Sapotaceae], Guatteria[Annonaceae], 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) (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 (Jaramilloet al. 2006). Slowdowns of diversification were mainly due to
decreases in speciation (Fig. 4 and 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
Páramo, 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, 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 (~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 et al. 2013).