92 SCIENCE HIGHLIGHTS: Sustaining Earth's Biodiversity

https://doi.org/10.22498/pages.25.2.92

Integrating paleoecology and phylogeography

reveals congruent bioclimatic regions
in the Brazilian Atlantic forest
Marie-Pierre Ledru1, A.C. Carnaval2, C.Y. Miyaki3 and “AF Biota” project participants4

The integration of paleoecological studies and genetic data from various Brazilian Atlantic forest organisms reveals
three main regions of contemporary spatial distribution of genetic diversity related to late Quaternary shifts in
monsoon activity.

The Atlantic forest is the second most biodi- climatic conditions. These geographical revealed by fossil pollen records (Ledru et
verse domain in Central and South America characteristics, combined with a wide alti- al. 2016) define three main areas within the
after the Amazonian rainforest. Its distribu- tudinal range, resulted in one of the highest Atlantic forest: North Atlantic Forest (NAF)
tion today has been strongly reduced to less degrees of species richness and rates of between 5° and 15°S, Central Atlantic Forest
than 16% of its original cover because of endemism on the planet (Joly et al. 2014). (CAF) between 15° and 23°S and South
intensive deforestation. The Atlantic forest Atlantic Forest (SAF) from 23° to 30°S. NAF
covers a large region along Brazil’s 4000 km Three paleoclimatic regions has a moist, cool, semi-deciduous forest
coast, from the Equator to 30°S (Fig. 1), and Modern regional climatic behaviors and restricted to coastal zones, lowland gallery
consequently is subject to a wide range of past forest expansion and regression phases forest and mountaintops. An evergreen
forest was well developed during the late
glacial instead of a deciduous forest (Fig. 2).
CAF is composed of coastal forest patches
of mainly dense evergreen forest, whereas
more inland areas are occupied by semi-
deciduous forests. The evolution of the CAF
shows several phases of expansion and
regression during the past 17 ka, which are
linked to the precession cycle of the insola-
tion (Ledru et al. 2009). SAF hosts Araucaria
or mixed evergreen forest characterized by
the presence of species adapted to cooler
and wetter climates. The SAF expanded
into the central region replacing the semi-
deciduous forest during the late glacial, and
since 3 ka is progressively expanding to the
south (Fig. 2). This observation is in agree-
ment with model predictions (Salazar et al.
2007). Two fossil pollen records from an
interior northern site (Caço Lake, currently
not forested) and from the central region
(Colônia, currently forested) indicate that the
expansion of the Atlantic forest cover was
out-of-phase between these two regions -
the northern site witnessed forest expansion
from 17 ka to the beginning of the Holocene,
while the central forest cover retracted
(Ledru et al. 2016). Additional paleoecologi-
cal datasets likewise indicate considerable
expansion of the (nowadays small-ranged)
northern forests during the deglaciation (17
to 12 ka; Wang et al. 2004).

Genetic diversity
Comparative phylogeographic data from
plants and animals provide a direct link
between asynchronous Late Quaternary
climatic shifts, the historical demography
of forest-depended species, and genetic
diversity patterns we observe today. If
animal populations in the south have been
Figure 1: Map showing the modern distribution of the Brazilian Atlantic forest with three main regions. NAF: tracking the Atlantic forest expansion
North Atlantic Forest; CAF: Central Atlantic Forest; SAF: South Atlantic Forest. in the late Holocene, then signatures of

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 SCIENCE HIGHLIGHTS: Sustaining Earth's Biodiversity 93

population expansion should be detected in

DNA sequence data from multiple species.
For instance, when a population becomes
isolated, the succession of the generations
within this population will generate new
DNA imprints that will differ from the DNA
imprints of the remote populations. On the
other hand, populations restricted to north-
ern, inland, highland sites must have been
exposed to forest contraction over the same
period and hence show genetic evidence
of strong population bottlenecks that will
reduce the diversity. NAF coastal popula-
tions, presumably exposed to permanently
humid conditions throughout the last 21 ka
(Carnaval and Moritz 2008; Carnaval et al.
2009), are expected to show high levels of
genetic diversity due to climatic stability.
Genetic data from coastal populations in the
SAF confirm this hypothesis and show much
lower levels of genetic diversity relative to
NAF coastal populations, tied to genetic
signatures of expansion and colonization
that date post LGM. This pattern is detected
in a vast array of forest taxa, including frogs,
lizards, birds, bats, and plants (e.g. Cabanne
et al. 2008; Carnaval et al. 2009; Fitzpatrick
et al. 2009; Martins et al 2009; Ribeiro et al.
2010; Fig. 2). Post-3 ka colonization of the
SAF is also seen in frogs and plants (Ramos
et al. 2009; Carnaval et al. 2009). In turn,
lineages restricted to mountaintop Holocene
forest refugia in inland northeastern Brazil
are narrowly endemic and show signatures
of recent bottlenecks, presenting low levels
of diversity (e.g. Ramos et al. 2009).

Climatic and diversity barriers

These asynchronous patterns of forest
movements over the last 17 ka were tracked
by various forest organisms, and largely
determined contemporary spatial patterns
of genetic diversity. Shift in monsoon activ-
ity, from north to south and south to north,
driven by the precession cycles, led to sig-
nificant differences in precipitation patterns
(Cruz et al. 2005) and, thus, in the tempo and
mode of rainforest contraction and expan-
sion in lowland and mid-altitude tropical Figure 2: Paleoecology and biodiversity in the Brazilian Atlantic forest with: (A) Changes in the spatial
areas. This mechanism must have triggered distribution of groups of pollen taxa from Araucaria and evergreen forests as a function of time and latitude
strikingly different demographic trajectories (modified from Ledru et al. 2016). Darker colors represent higher pollen concentrations. (B) Network showing
relationships among mitochondrial DNA sequences of a bird species (modified from Cabanne et al. 2008). Each
between northern, central and southern spe-
circle represents a sequence and their sizes are proportional to their frequency in the sample, the length of the
cies pools within forests distributed among
lines represents the number of differences, and colors represent main areas (NAF, CAF and SAF). Note that two
this gradient. Such tracking of forested envi- subgroups were distinguished within the SAF, but factors other than the monsoon shifts may have caused this
ronments by whole tropical assemblages or separation.
species pools should largely explain contem-
porary patterns of genetic diversity in these Carnaval C et al. (2009) Science 323: 785-789
tropical forest dynamics and the species-
tropical regions. In the Brazilian Atlantic
level tolerances to climate change. Cruz et al. (2005) Nature 434: 64-66
forest, proposed forest refugia and areas of
Fitzpatrick SW et al. (2009) Mol Ecol 18: 2877-2896
high genetic diversity and endemism match
areas within the sea-saw monsoonal sector AFFILIATIONS Joly C et al. (2014) New Phytol 204: 459-473
that were permanently moist over the last 17
1
Institut de Recherche pour le Développement (UMR Ledru M-P et al. (2009) Palaeogeogr Palaeoclimatol
ISEM), University of Montpellier, France
ka. The three bioclimatic regions evidenced Palaeoecol 271: 140-152
2
Department of Biology, City University of New York,
by phylogeography are located in the three Ledru M-P et al. (2006) Quat Sci Rev 25: 1110-1126
USA
paleoecological and paleoclimatic regions 3
Departamento de Genética e Biologia Evolutiva, Ledru M-P et al. (2016) Biotropica 48: 159-169
revealed by pollen records and related to Universidade de São Paulo, Brazil Martins FM et al. (2009) BMC Evol Biol 9: 294
past fluctuant monsoon activity at these 4
Project “AF Biota” FAPESP (BIOTA 2013/50297-0), NSF
Ramos ACS et al. (2009) J Heredity 100: 206-216
latitudes. (DEB 1343578) and NASA
Ribeiro RA et al. (2010) Heredity 106: 46-57
CONTACT
The use of plant fossil information and Marie-Pierre Ledru: [email protected]
Salazar LF et al. (2007) Geophys Res Let 34: L09708
genetic data from forest species to illustrate Wang et al. (2004) Nature 432: 740-743
past climatic shifts and their associated re- REFERENCES
sponses from the fauna and flora of eastern Cabanne SG et al. (2008) Mol Phylogenet Evol 49:
South America question the timescale and 760-773
pace of diversification, the role of refugia in Carnaval AC, Moritz C (2008) J Biogeogr 35: 1187-1201

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