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 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 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 Jret al. 2004; Hoorn et al. 2010; Antonelli & Sanmartín
2011; Rull 2011a).
A long-held tenet was that the outstanding levels of Neotropical
diversity were mainly generated during the Quaternary (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 et al. 2010) and fossil studies
showing a fossil record significantly more diverse in the Eocene than
posteriorly (Jaramillo et al. 2006). Although recent studies show
that modern climate (Moritz et al. 2000; Rull 2011a; Rowanet al. 2019) and intrinsic biological traits (Smith 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 (Mittelbachet al. 2007; Hoorn et al. 2010; Rull 2011a; Antonelliet 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 et al. 2010; Luebert &
Weigend 2014; Antonelli et al. 2018a; Esquerré et al.2019). Andean uplift began in the Central Andes ~65 Myrs
ago (Mya) as a result of subduction of the Nazca plate along the Pacific
margin, and in the Northern Andes ~23 Mya, with the
collision of the Pacific plate. Uplift then intensified
~12-4.5 Mya (Garzione et al. 2008; Hoorn et
al. 2010; Chen 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 et al. 1995; Armijo 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 (Blisniuket al. 2005; Hoorn et al. 2010, 2017). This tectonic
rearrangement also led to the closure of the Central American Seaway
~10 Mya (Jaramillo 2018).
The dynamic landscape caused by the Andean uplift has been postulated to
have a major effect on Neotropical diversification by (i)increasing habitat and environmental heterogeneity (today all major
biomes appear in the region, e.g. tropical forests, deserts, and
high elevation grasslands), (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 (Flantuaet al. 2019), and by (iii) creating the longest
latitudinally-elongated corridor for biotic montane dispersal (Antonelliet al. 2009; Luebert & Weigend 2014). As such, Andean uplift has
been associated with the explosive radiation of plants, insects, and
tetrapods (Weir 2006; Drummond et al. 2012; Lagomarsino et
al. 2016; Pérez-Escobar et al. 2017; Pouchon et al. 2018;
Chazot et al. 2019; Esquerré et al. 2019), and with
increased rates of biotic interchange (Santos et al. 2009;
Fjeldså et al. 2012; Antonelli et al. 2018c; Baconet al. 2018).
Analyses of the fossil record also suggest that Neotropical diversity
has been strongly linked to temperature (Hoorn et al. 1995;
Jaramillo 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)
~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 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 (Simonet al. 2009; Antoine et al. 2013). These past climatic
events are also thought to have shaped Neotropical diversification
(Pinto‐Ledezma et al. 2017). Plant diversity inferred from fossil
morphotypes increased with warming periods during the Eocene, and
decreased sharply with subsequent cooling (Hoorn et al. 1995;
Jaramillo et al. 2006). Quaternary glacial cycles have been
considered to promote fragmentation in rainforest ecosystems and
high-altitude habitats (e.g. through altitudinal shifts in Andean
vegetation zones), which in turn contributed to geographical isolation
and diversification (Haffer 1969; Rull 2011a; Flantua 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 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 et al. 2013, 2019). Some studies have focused on
particular Neotropical clades to infer their triggers of diversification
(Lagomarsino et al. 2016; Esquerré 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 ~60% of all estimated tetrapods
and ~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.