Pleistocene climatic instability drove the historical distribution of forest islands in the northeastern Brazilian Atlantic Forest

Pleistocene climatic instability drove the historical distribution of forest islands in the northeastern Brazilian Atlantic Forest

Palaeogeography, Palaeoclimatology, Palaeoecology 527 (2019) 67–76 Contents lists available at ScienceDirect Palaeogeography, Palaeoclimatology, Pal...

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Palaeogeography, Palaeoclimatology, Palaeoecology 527 (2019) 67–76

Contents lists available at ScienceDirect

Palaeogeography, Palaeoclimatology, Palaeoecology journal homepage: www.elsevier.com/locate/palaeo

Pleistocene climatic instability drove the historical distribution of forest islands in the northeastern Brazilian Atlantic Forest

T

Mario Henrique Barros Silveiraa,b, Rilquer Mascarenhasa,b, Domingos Cardosoa, ⁎ Henrique Batalha-Filhoa,b, a

National Institute of Science and Technology in Interdisciplinary and Transdisciplinary Studies in Ecology and Evolution (INCT IN-TREE), Instituto de Biologia, Universidade Federal da Bahia, Brazil b Laboratório de Evolução e Biogeografia, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão de Jeremoabo, s.n., Ondina, Salvador, Bahia 40170-115, Brazil

ARTICLE INFO

ABSTRACT

Keywords: Ecological niche modeling Phylogeography Forest enclaves Neotropics

To investigate the past spatial dynamics of Atlantic Forest (AF) ‘island-like’ enclaves in northeastern Brazil, we employed ecological niche modeling (ENM) using a set of georeferenced records of 13 woody plant species. ENMs were constructed using the Ensemble forecasting approach and were projected into past climatic conditions for the last interglacial period (LIG, 120 kyr), last glacial maximum (LGM, 21 kyr), and the Middle Holocene (MH, 6 kyr). Our results suggest an expansion of wetter forests during the LGM into areas currently covered by the Caatinga seasonally dry woodlands, with recent retraction to the current distribution. Central AF islands located south of the São Francisco River underwent a different history compared to Northern AF islands north of this river: the former were mostly connected to coastal AF since the LIG (with a very recent separation), whereas the latter presented a more dynamic historical distribution. Results reveal contrasting spatiotemporal histories of forest instability and isolation across the various enclaves, supporting three main biogeographic hypotheses: i) moderate connectivity with coastal AF and a recent population bottleneck in the Araripe and Pernambuco/Paraíba enclaves, ii) low connectivity to, and long-term isolation from, other enclaves, as well as recent population bottleneck, in the northernmost North Ceará enclaves; and iii) high connectivity with coastal AF and recent population expansion in the southernmost Chapada Diamantina enclaves. Future comparative phylogeography studies will largely aid in assessing the herein proposed biogeographic scenarios during the highly dynamic recent history of the AF enclaves.

1. Introduction Depicting the historical processes that drove diversification in megadiverse biomes is a central question in evolutionary biogeography (Barrow et al., 2017), especially in climatically and geotectonically complex regions (Rull, 2008, 2013). In the Neotropics, where several evolutionary scenarios are often assumed to be involved in the species build-up, patterns and processes of diversification still remain poorly understood (Moritz et al., 2000; Pennington et al., 2006; Antonelli and Sanmartín, 2011; Rull, 2011). Among the Neotropical biomes, the highly threatened lowland and montane rainforests of the Atlantic Forest (AF) biodiversity hotspot (Myers et al., 2000) exhibit an exceptionally high number of endemic species with a complex evolutionary history (Galindo-Leal and Câmara, 2003; Ribeiro et al., 2011b). Therefore, the AF provides an excellent opportunity to look at how

historical diversification processes have shaped the Neotropical biodiversity. Phylogeographic studies to date have suggested a key role of late Pleistocene climate changes on the historical demography and population divergence of different AF taxa, including bees (BatalhaFilho et al., 2010), amphibians (Carnaval and Moritz, 2008; Carnaval et al., 2009; Carnaval et al., 2014), birds (Cabanne et al., 2007; d'Horta et al., 2011; Batalha-Filho and Miyaki, 2016), bats (Martins et al., 2009; Pavan et al., 2011), sloths (Moraes-Barros et al., 2006; Silva et al., 2017), and trees (Ribeiro et al., 2011a; Dantas et al., 2014). However, incongruent phylogeographic patterns regarding time and mode of diversification have also been revealed, including vicariant history prior to the late Pleistocene (Grazziotin et al., 2006; Thomé et al., 2010; Amaral et al., 2013) and demographic stability or expansion through glacial maximum periods (Batalha-Filho et al., 2012; Cabanne et al., 2013; Leite et al., 2016). In these cases, contrasting biogeographic

⁎ Corresponding author at: National Institute of Science and Technology in Interdisciplinary and Transdisciplinary Studies in Ecology and Evolution (INCT INTREE), Instituto de Biologia, Universidade Federal da Bahia, Brazil. E-mail address: [email protected] (H. Batalha-Filho).

https://doi.org/10.1016/j.palaeo.2019.04.028 Received 7 October 2018; Received in revised form 26 April 2019; Accepted 26 April 2019 Available online 29 April 2019 0031-0182/ © 2019 Elsevier B.V. All rights reserved.

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explanations have centered on recent tectonism in the eastern Brazilian Shield (Thomé et al., 2010) or possible dispersal onto the exposed continental shelf during glacial periods (Leite et al., 2016). Among several approaches (e.g., genetic and paleo-records) that can be used to test biogeographic hypotheses (Gavin et al., 2014; RocesDiaz et al., 2018), the projection of ecological niche models onto paleoclimatic conditions has largely assisted in the understanding of the evolutionary history in the AF domain (e.g., Carnaval and Moritz, 2008; Carnaval et al., 2009). In phylogeographic studies, ENMs allow the recovering of ecological data independent from genetic information, enhancing a comparative data-driven hypothesis testing (AlvaradoSerrano and Knowles, 2014). Studies using this approach have insightfully modeled the past distribution of the AF and revealed ecological breaks dividing northern, central, and southern regions during glacial periods (Carnaval and Moritz, 2008; Carnaval et al., 2014), which exhibit coincidence with the location of major rivers: the Doce River separates southern and central AF, whereas the São Francisco River separates central and northern AF. This division is in accordance with some phylogeographic discontinuities (Cabanne et al., 2008; Carnaval et al., 2009; Ribeiro et al., 2011a, b; d'Horta et al., 2011; Maldonado-Coelho, 2012; Batalha-Filho and Miyaki, 2016) and the models also predict that the central AF was more paleoclimatically stable (Carnaval and Moritz, 2008), whereas southern AF exhibited more instability during climatic changes across Pleistocene cycles (Behling, 2002; Ledru et al., 2005; Carnaval and Moritz, 2008; Carnaval et al., 2009; Costa et al., 2018). Nonetheless, these historical demographic predictions were not always supported in later studies (e.g. Amaro et al., 2012; Batalha-Filho et al., 2012; Cabanne et al., 2013; Brunes et al., 2015; Leite et al., 2016), suggesting little predictive power in the models generated so far. Despite advances in the comprehension of AF biogeography, most studies have focused thus far on central and southern AF. Few studies have investigated taxa distributed in the northern AF (Carnaval and Bates, 2007; Carnaval and Moritz, 2008; Cabanne et al., 2008; d'Horta et al., 2011) and how the late Pleistocene climatic instability might have affected forest distribution in this region. Interestingly, the present-day island-like discontinuous distribution of the northern AF forests greatly contrasts with the large expanses of continuous southern AF forests (Fig. 1A). The northern AF includes a more continuously distributed forest through Brazilian coastline and disjunct, isolated patches or enclaves of “rainforest islands” scattered in higher elevations within the seasonally dry forest and woodland biome of the Caatinga domain (Andrade-Lima, 1982; Tabarelli and Santos, 2004; Rocha et al., 2007; Santos et al., 2007; Queiroz et al., 2017). Several floristic studies have suggested an Amazonian influence, i.e., a significant presence of typical Amazonian species, on the plant community assembly of northern AF enclaves (Andrade-Lima, 1982; Tabarelli and Santos, 2004; Santos et al., 2007). A recent study also showed the strong contribution of the main coastal AF as a source of species, influencing the community composition in such enclaves (Silva-de-Miranda et al., 2018). The historical assembly of the enclaves local community has largely been discussed in terms of how Pleistocene glacial cycles shaped the distribution of these enclaves through cyclical Amazonian and Atlantic forest expansion and retraction during the Quaternary (Auler et al., 2004). Indeed, paleopalynological records along this period revealed cold and humid events in currently semiarid areas (Behling et al., 2000; Ledru et al., 2007; Ledru et al., 2016), which suggest the occurrence of wet forested areas during the late Pleistocene (Oliveira et al., 1999; Behling et al., 2000; Auler and Smart, 2001; Auler et al., 2004; Wang et al., 2004). Investigating how Pleistocene glacial cycles shaped the historical distribution of rainforest enclaves across the largely neglected northern AF region will also improve our understanding of the impact of climate change on forest dynamics and spatial distribution of genetic diversity. Furthermore, the island-like nature of these natural forest enclaves represents a distinctive evolutionary theater for investigating how the historical dynamics of forest range size, contraction, and

expansion promote biological diversification. Herein we investigated the role of Pleistocene and recent Holocene climatic fluctuations on shaping the distribution of forest enclaves in the northern AF. To shed light in this biogeographic scenario, we developed ecological niche models to reconstruct the spatiotemporal distribution of the northern AF during the last 121 kyr. We specifically addressed (i) whether forest enclaves were connected among them and to the coastal AF during past periods and (ii) whether the degree of such connection changed during the late Pleistocene. Finally, we summarized whether, where, and when connection pathways occurred among northern AF enclaves and present hypotheses of past connections among enclaves as well as testable phylogeographic predictions for each hypothesis. These predictions were compared with studies on paleopollen, speleothems and geochemical analyses of sediment content, as well as the still sparsely available phylogeographic data. 2. Materials and methods 2.1. Study area Rainforest enclaves in northeastern Brazil to the north of São Francisco River are locally called Brejos Nordestinos (herein after BN) (Andrade-Lima, 1982) and were divided here in three sets according to their regional location or topographic denomination (Fig. 1): the BN associated with Meruoca, Itapipoca, Maranguape, Baturité and Itatira plateaus (the Northern Ceará enclaves), the BN associated to the Borborema plateau (the Pernambuco/Paraíba enclaves) and the BN associated with the Araripe plateau (Araripe enclaves). We also investigated forest enclaves below the São Francisco river, in central AF; these occur mostly as seasonally dry, but also highly wet forests that are mainly distributed on the east side of the Chapada Diamantina, which corresponds to the northern portion of the Espinhaço mountain range, in the central region of state of Bahia (Rocha et al., 2007). Floristic surveys in such rainforest enclaves have often revealed new plant species and significantly higher diversity than the surrounding Caatinga seasonally dry woodlands (e.g., Porto et al., 2004; Cardoso and Queiroz, 2008). The maintenance of such higher diversity and endemism is likely because of the particular conditions of these rainforest enclaves where they are isolated at higher elevations mostly between 500 and 1300 m and under higher mean annual precipitation (sometimes well above 1200 mm) (Andrade-Lima, 1982; Rocha et al., 2007). This sharply contrasts with the harsh conditions of erratic precipitation and severe drought that can sometimes extend over consecutive years in the adjacent lowland Caatinga dry vegetation, largely limiting the dispersal of possible immigrants from the rainforest enclaves (Oliveira-Filho et al., 2013; Queiroz et al., 2017). 2.2. Input data for model calibration To model forested habitat, we used a set of geographic referenced records of 13 woody plant species ecologically associated to the AF. Considering the high vegetation heterogeneity across our study area (Fig. 1), where environmental conditions may change across small distances around the enclaves, due to variation in elevation, we chose to calibrate our models based on the knowledge of plant species exclusive to forest habitats, instead of randomly sampling points from within a polygon. This latter approach could yield spurious data when occurrence points are sampled near the polygon edge (where climatic conditions could resemble more the Caatinga open vegetation surrounding the forest than the forest itself). By restricting our occurrence points to recorded occurrence of forest-specialist plant species, we avoid this bias and achieve more accurate models. The different species were combined in a single file to represent points of distribution of northern AF which were used as input of modeling. Our selected species encompassed different families, including an arborescent fern Cyathea delgadii Sternb. (Cyatheaceae), a gymnosperm Podocarpus sellowii 68

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Fig. 1. The ‘island-like’ rainforest enclaves of the Brazilian Atlantic Forest domain (green shading) are scattered at higher elevations within the Caatinga domain (grayish shading), where the harsh environment of seasonally dry forests and woodlands predominates (representative images C, F, and G). The focus of this study is set on the main northern Atlantic Forest enclaves that are located in the following regions within red polygons (representative images A, B, D, and E): 1) Northern Ceará enclaves, 2) Pernambuco/Paraíba enclaves, 3) Araripe Complex enclaves, and 4) Chapada Diamantina enclaves. All other acronyms refer to Brazil's political subdivision in states. Photos by Mario H. B. Silveira (A, Serra do Baturité-CE; and B, interior of a forest enclave at São Vicente Ferrer-PE) and Domingos Cardoso (C, seasonally dry woodland near Jaguarari-BA; D, Serra do Orobó in Itaberaba-BA; E, interior of the forest enclave at Serra do Orobó; F, seasonally dry woodland on limestone outcrop at Morro do Chapéu-BA; and G, seasonally dry forest or arboreal Caatinga near Paramirim-BA). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Klotzsch ex Endl. (Podocarpaceae), and mostly angiosperms: Schefflera morototoni (Aubl.) Maguire, Steyerm. & Frodin (Araliaceae), Aspidosperma discolor A.DC. (Apocynaceae), Ocotea glomerata (Nees) Mez (Lauraceae), Henriettea succosa (Aubl.), DC., Miconia nordestina R.Goldenb. & E.C.O.Chagas (Melastomataceae), Ficus arpazusa Casar. (Moraceae), Myrcia sylvatica DC. (Myrtaceae), Cassia ferruginea Schrad. ex DC., Dimorphandra jorgei M.F.Silva, Hymenolobium janeirense Kuhlm., and Ormosia fastigiata Tul. (Leguminosae). These selected species are ecologically representative of the semideciduous to humid settings in the northern AF, including a congruent distribution with the current projections of the forest enclaves (see Results and Fig. 2B). Additionally, these species are well collected and represented in herbarium collections. Occurrence points as vouchered herbarium specimens for the abovementioned plant species (Table S1 in Appendix S1) were retrieved from the publicly available databases of the Global Biodiversity Information Facility (www.gbif.org/) and speciesLink (www.splink.cria.org.br/). All herbarium records were taxonomically vetted in order to correct or exclude erroneously identified and georeferenced records that are widely common in online tropical plant collections (Goodwin et al., 2015; Cardoso et al., 2017). We accounted

for the effect of spatial autocorrelation by calculating the geographic distance among points and excluding those occurring in < 10 km from each other, performed in the software R v. 3.4 (R Core Team, 2017) using a custom-made script. This is a simple approach to reduce the climatic correlation among points to close proximity (Dormann et al., 2007; Oliveira et al., 2014), which can falsely inflate model accuracy. A total of 302 occurrence points was used for model calibration after correcting erroneous specimen records and accounting for spatial autocorrelation. Environmental variables were obtained from the WorldClim online database (Fick and Hijmans, 2017; http://www.worldclim.org/), available for the Current (interpolations of observed data, representative 1960–1990), Middle Holocene (MH – approximately 6 kyr), LGM (approximately 18–21 kyr) and Last Inter Glacial (LIG – approximately 120 kyr) periods. We downloaded different Atmospheric Oceanic Global Circulation Model (AOGCMs) for a period, when available, and calculated the mean value for each cell in the spatial variable using the raster package (Hijmans and Etten, 2014) in R. We chose this approach in order to yield a single biogeographic hypothesis for our model system, instead of a different hypothesis for each AOGCM 69

Fig. 2. Modeled ranges of northern Atlantic Forest enclaves under narrow distributional definitions for current conditions, 6 kyr (Middle Holocene), 21 kyr (Last Glacial Maximum), and 120 kyr (Last Interglacial) climatic scenarios. Gray scale maps represent binary suitability maps based on a threshold of the presence or absence of modeled enclaves; white circles in binary projection of Present Day conditions represent the occurrence records of plants species (Appendix S1) while yellow circles represent paleobiological evidences of wet conditions during the Quaternary (see Table S2). Color maps represent suitability maps, where the warmer colors of the logistic output format correspond to regions with a higher probability of Atlantic Forest enclaves. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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(Diniz-Filho et al., 2009). We obtained the mean value calculation on the original climatic variables (instead of calculation on the final suitability modeled by algorithms) to decrease the amount of mathematically modeled information used to estimate past distribution. Calculating the mean based on past climatic variables means a calculation on values deriving from one modeled value (the AOGCM), whereas calculating the mean based on final suitability values (which would be another alternative to combine different AOGCMs in a single biogeographic model) means a calculation on values that were modeled (by ENM algorithms) from other modeled values (i.e., the AOGCMs). As each model brings a degree of simplification from empirical data (e.g., Giere, 1999), we chose to reduce the degree of this simplification implemented in modeling algorithms. Only the periods MH and LGM have more than one AOGCM available, and we restricted our AOGCM dataset to those present in both these periods: CCSM4, MIROC-ESM and MPI-ESM-P, developed through Coupled Model Intercomparison Project Phase 5 (http://cmip-pcmdi. llnl.gov/cmip5/). Information on the current climate is based on the interpolation of observed data, between 1960 and 1990, whereas LIG climatic data is based on Otto-Bliesner et al. (2006). We used bioclimatic layers in 2.5 arc-minutes resolution (4.5 km × 4.5 km ~ 16 km2 in Equator) and they were cropped to a geographic extent between the coordinates −44.71 (maximum longitude), −33.77 (minimum longitude), −20.00 (maximum latitude) and −2.20 (minimum latitude). This reduction in the extent assures a correct characterization of the background environmental characteristics to be used in model calibration, leading to better ENMs performance and accuracy (Anderson and Raza, 2010). To minimize collinearity among the variables in the construction of models, we performed a factor analysis on the 19 variables available in the WorldClim database (Terribile et al., 2012; Oliveira et al., 2014). Five variables were then retained (Table S1 in Appendix S2): mean diurnal range, isothermality, mean temperature of warmest quarter, precipitation of wettest month and precipitation of driest month, which accounted for 90% of the total variation in the original dataset.

evaluated the maps generated by ENMs, considering binary and suitability continuous maps. For each period, we recorded (i) whether enclaves were connected or not; (ii) which enclaves were connected, as well as where and when connection pathways occurred; and (iii) whether forest areas were larger or smaller than current range size. Additionally, we evaluated range size changes across different times, comparing the maps from each period with the maps from the next period (i.e., comparing LIG with LGM; LGM with MH; and MH with current period). This allowed us to derive biogeographic predictions for the northern AF, regarding genetic diversity, levels of connectivity and demographic fluctuations of populations. The hypothetical biogeographic model was validated by geological data (paleopollen and speleothems) and phylogeographic studies, available for the northern AF. 3. Results The modeled distribution of the set of 13 forest plant species was effective in reflecting the current distribution of the rainforest enclaves in the northern AF (Fig. 2A). The model shows separate distribution between Chapada Diamantina and the coastal AF, with small connectivity in the southeastern area of this region, across upper Paraguaçu River basin. In the BN, similar disjunct distribution was also recovered, with Pernambuco/Paraíba enclaves as isolated forest patches, as well as North Ceará enclaves, where the isolation was more evident. Model projections for the past climatic conditions revealed differences with respect to present-day distribution of forest enclaves. During the LIG, forested areas were mostly restricted to the coast from northern of Rio Grande do Norte to southern Bahia; forests were present in the interior region, encompassing present Chapada Diamantina and most of the interior of Bahia state east of the São Francisco River. In areas north of the São Francisco River, there was a disjunction between main AF and Araripe enclaves, as well as between main AF and North Ceará enclaves, with these latter showing great reduction in size. Our maps from the LGM (Fig. 2C) revealed forest expansion in areas north of the São Francisco River, connecting most areas currently occupied by Caatinga seasonally dry woodlands in the states of Paraiba, Pernambuco and Rio Grande do Norte, as well as southern Ceará in the Araripe enclaves. This widespread expansion of rainforests during the LGM created connection pathways among coastal AF and forest islands of the Pernambuco/Paraíba and Araripe enclaves, a connection that does not seem to have happened during the LIG (Fig. 2D). On other hand, the North Ceará enclaves remained separated and isolated during this period (although also with larger range sizes than those seen in current and previous LIG climatic conditions, Fig. 2C). In areas south of the São Francisco River, Chapada Diamantina forests and coastal AF remained connected during the LGM, but retracted northward from their previous LIG distribution (which extended southward reaching the Doce River). Finally, all enclaves became effectively isolated only in the MH (Fig. 2B), except for North Ceará enclaves which was fairly isolated since the LIG. Also during this period, no rainforests were observed in the Araripe enclaves, while in the Chapada Diamantina forests were reduced, probably reaching its current distribution very recently (Fig. 2A). Our maps suggest significant changes in range size in most enclaves, which probably affected the demographic history of populations resident in these areas: coastal forests north of the São Francisco River, as well as Pernambuco/Paraíba and Araripe enclaves, were greatly reduced from LGM distribution until reaching their current distribution. Interestingly, North Ceará enclaves remained relatively stable and isolated in all modeled periods since the LIG. Chapada Diamantina enclaves show a recent increase in range size, from MH to the current period. Additionally, the southernmost coastal forests reached the Doce River during the LIG, but reduced to southern Bahia during the LGM. Expansion towards the Doce River occurred again from the MH into the current period (although not as extensive as the LIG distribution).

2.3. Model calibration Occurrence and environmental data were implemented in modeling algorithms to estimate a climatic niche for the entity being modeled (northern AF), which was then projected onto the geographical space in current and past climatic conditions. We used the package BIOMOD (Thuiller et al., 2016) in R and implemented the Ensemble forecasting approach (Araújo and New, 2007), which combines different modeling algorithms while accounting for variation among their results and statistical support for each model. We implemented all 10 algorithms: Generalized Linear Model, Generalized Additive Model, Generalized Boosting Model, Classification Tree Analysis, Artificial Neural Network, Surface Range Envelop – BIOCLIM, Flexible Discriminant Analysis, Multiple Adaptive Regression Splines, Random Forest and Maximum Entropy. Model calibration was based on 20 replicates for each algorithm: the first ten replicates randomly split occurrence points into training data (75%) and testing data (25%) for model evaluation (partitioned models) and the remaining ten replicates were performed using the total data set (full models). Evaluation was based on the TSS (True Skill Statistic; Allouche et al., 2006), and full models presenting TSS > 0.9 were then used to generate the final ensembled outputs. The TSS method was also utilized to convert suitability continuous maps into presence-absence maps. We used DIVA-GIS v.7.5 (www.diva-gis.org) to edit all the consensus projections of the models generated. 2.4. Defining a testable biogeographic hypothesis To build a hypothetical biogeographic model we qualitatively 71

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4. Discussion

Our resulting paleoclimatic model also revealed pronounced changes in the forest range during the LIG. Areas located north of the São Francisco River were generally similar to their current distribution. Notwithstanding, the model suggests large continuous forest expanse at south of the São Francisco River, covering large areas in Bahia state southward until the Doce River (Fig. 2D). This pattern is not similar to the currently observed forest distribution and contrasts the general assumption that interglacial periods would show forest distribution similar to what is seen today (Anderson et al., 2007; Bush and Metcalfe, 2012). In this sense, speleothem data indeed indicate wetter LIG conditions inner in Bahia, enabling the support of rainforests (Wang et al., 2004; Stríkis et al., 2018) and further supporting the high stability of forests in the so-called Bahia refugium. During the MH period, on the other hand, there is great forest retraction from the previously expanded distribution during the LGM (Fig. 2B). This retraction is also supported by evidences of paleopollen (Oliveira et al., 1999; Behling et al., 2000) and sediment analyses (Sifeddine et al., 2003; Pessenda et al., 2010), which suggest expansion of savanna and scrub vegetation during dry and warm phases of the MH, marking the expansion and consolidation of the Caatinga seasonally dry woodlands and the savanna-like vegetation of the Cerrado domain. Our models exhibited a more pronounced forest retraction within the Caatinga seasonally dry woodlands to the north of São Francisco River, around the Araripe and North Ceará enclaves, which agrees with sediment geochemical analyses from this and nearby regions (Pessenda et al., 2004; Pessenda et al., 2010). The Chapada Diamantina enclaves also underwent retraction, but they were not completely isolated, remaining connected to coastal forests possibly via gallery forests which exist along the Paraguaçu River basin (Fig. 2B). Finally, our models suggest a high connection (and therefore high levels of gene flow) among northern rainforest enclaves to the north of São Francisco River during the LGM, excluding the North Ceará forest complex (Fig. 2C). Species distribution in these enclaves and coastal AF also support the historical connections suggested here. A recent, late Pleistocene wider connection between the AF and lowland Amazon rainforests, through the expansion of forest enclaves within the presentday Caatinga seasonally dry woodlands, was indirectly demonstrated by distribution data and divergence time estimates in birds (BatalhaFilho et al., 2013). Our models add new information about such connectivity, showing different histories of recent enclaves connection: whereas enclaves in the Araripe and Pernambuco/Paraíba regions showed fluctuating levels of connectivity across the periods modeled, the North Ceará enclaves remained fairly separated at least since the LIG.

4.1. Supporting evidence on the biogeographic history of the northern rainforest enclaves Using a paleoclimatic modeling approach, we revealed different biogeographic histories in distinct regions of northern and central AF, particularly with respect to the rainforest enclaves in the north and south of the São Francisco River. The first main discovery revealed here is that currently isolated rainforest enclaves were connected during the LGM. While LGM conditions drove some degree of fragmentation in the southern AF (Carnaval and Moritz, 2008; Carnaval et al., 2009), they seem to have allowed expansion of northern AF, connecting the currently isolated rainforest enclaves. This scenario agrees with geological evidences from speleothems (Auler and Smart, 2001; Auler et al., 2004; Wang et al., 2004; Cruz Jr et al., 2007), paleopalynology (Oliveira et al., 1999; Behling et al., 2000; Sifeddine et al., 2003; Ledru et al., 2005; Dupont et al., 2010; Bouimetarhan et al., 2018), and sediment analyses (Jacob et al., 2007; Pessenda et al., 2010), which suggest wetter conditions in many present-day seasonally dry areas through the Caatinga domain. This overall rainforest expansion in northeastern Brazil during the LGM is suggested to be strongly related to the southward displacement of the Intertropical Convergence Zone, especially by the end of this period (Peterson et al., 2000; Wang et al., 2004; Jacob et al., 2007), which promoted humid conditions in this region and influenced South American summer monsoon (Zhou and Lau, 1998; Dupont et al., 2010; Stríkis et al., 2018; Bouimetarhan et al., 2018). However, the spatially scattered paleoecological records do not allow inferences about the extent of the forest expansion into present-day Caatinga areas. By directly modeling the historical processes through ENM approach, we are able to reconstruct here a more detailed biogeographic scenario (Svenning and Skov, 2004, 2007; Svenning et al., 2008). To the north of the São Francisco River, expansion of forests during LGM occurred mainly on the coast (both inward and into the continental shelf) and around the Araripe enclaves region. Contrastingly, to the south of the São Francisco River, forests occupied all of Chapada Diamantina and most Caatinga seasonally dry areas in the state of Bahia. Forests around current North Ceará forest complex showed a lesser degree of extension, not connecting with the other enclaves (Fig. 2). The expansion of forest areas during the LGM is not in agreement with the largely discussed classic biogeographic hypothesis of refuge formation in Neotropical forests (e.g., Connor, 1986; Mayr and O'Hara, 1986; Carnaval and Moritz, 2008), which postulates forested regions retracted and fragmented during cold and dry periods such as the LGM. Recent evidences from genetic data and paleomodeling contradict this classic idea by showing a much-expanded AF during the LGM (Cabanne et al., 2016; Leite et al., 2016). When compared with previously published bioclimatic modeling of the AF (Carnaval et al., 2014), the models generated here add support to the idea of a large forested area in Bahia state during the LGM (previously called “the Bahia refugium”). Additionally, the results also suggest that northern AF (i.e., forests located north of the São Francisco river) was highly unstable, which is a pattern similar to the one recovered for the southern AF (i.e., located south of the Doce river). Both these areas presented climatically stable zones during glacial periods (support for southern AF in Carnaval et al., 2014, and for northern AF in the models here presented). As suggested by Carnaval et al. (2014), southern AF forests are currently in what they named a “retracted phase” of the glacial cycles, i.e., southern forests have expanded during glacial maxima and are currently contracted. A similar pattern probably depicts the historical distribution of the forests located to the north of the São Francisco River: expansion during LGM (to a lesser degree in North Ceará enclaves) and fragmentation in interglacial periods. Therefore, both southern and northern AF might have undergone less stable and more dynamic range shifts during late Pleistocene glacial cycles, when compared to central AF.

4.2. Distinct evolutionary histories in the northern Atlantic Forest enclaves Previous paleoclimatic modeling on the historical distribution of the AF had focused on both the entire domain (Carnaval and Moritz, 2008; Carnaval et al., 2014) or on particular species (Porto et al., 2013; Cabanne et al., 2016). By focusing on the northern AF biogeographic region, distinct histories across the forest enclaves were unfolded here. Results from our models suggest that the forest enclaves in northern and central AF encompass three biogeographic regions with evolutionarily distinct histories (Fig. 3): the Araripe and Pernambuco/Paraíba enclaves, the northernmost North Ceará enclaves and the southernmost Chapada Diamantina enclaves. The Araripe and Pernambuco/Paraíba enclaves regions exhibited a history of fluctuating levels of connectivity, with high connectivity during the LGM and isolation in other periods. The greatest degree of forest isolation is seen at Araripe enclaves, whereas the Pernambuco/ Paraíba enclaves were overall less isolated across modeled periods, although they also showed fluctuating levels of connectivity. Additionally, a great retraction in forest range size is seen from the LGM towards current climatic conditions. The models also suggest that the MH period is a climatic extreme promoting forest retraction (the other 72

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Fig. 3. Newly proposed biogeographic hypotheses of the connectivity and demography of populations in the rainforest enclaves. The map to the right shows the study area, highlighting the enclaves (green shading within red polygons) currently isolated within the Caatinga domain (grayish shading) and coastal rainforests of the northern Atlantic Forest (green shading). NC = North Ceará enclaves; APP = Araripe/Paraíba/Pernambuco complex enclaves; CD = Chapada Diamantina enclaves. Arrows indicate connectivity between areas: blue arrows indicate high and ongoing connectivity, whereas black arrows indicate intermediate levels of connectivity, occurring only during a few periods in the past. The dashed line indicates the division between what is commonly known as northern and central Atlantic Forest, marked by the location of the São Francisco River. The diagram to the left represents the three main evolutionary predictions for populations existing in the enclaves areas. The width of bars indicates population size across different times (indicated by dashed lines and their respective ages; kya = thousands years ago). Population sizes (width of bars) are not comparable among enclaves. Red bars are used in NC to indicate low to no connectivity with other areas across most of the time modeled in this study. Green bars are used to indicate the opposite scenario, i.e., high connectivity between the respective enclaves and other forested areas. Colored arrows indicate the genetic predictions for populations in each enclave: Fst was used to indicate the levels of genetic differentiation when comparing the enclaves populations with populations from any other areas; D represents demographic scenarios, i.e., either population expansion (arrow pointing up) or reduction (arrow pointing down). In this sense, NC populations would show high Fst and signatures of population bottleneck, APP populations would show low Fst and signatures of population bottleneck and CD populations would show low Fst and signatures of recent expansion. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

extreme being the LGM period, promoting the largest forest range sizes), since forests seem to have slightly expanded from the MH period into current conditions. Given the short timespan between MH and current conditions, as well as the much larger range size change from LGM to MH, we suggest that the signature of population bottleneck will be more evident than any signal of recent and small population expansion. Therefore, populations inhabiting Araripe, Paraíba and Pernambuco enclaves will probably exhibit a signature of recent population size reduction. The few studies addressing phylogeographic patterns in northern AF frog (Carnaval and Bates, 2007) and bird species (Cabanne et al., 2008; d'Horta et al., 2011) found little isolation of Pernambuco/Paraíba enclaves and coastal forests, which agrees with our model of recent LGM connection. We suggest that populations in North Ceará enclaves will show signatures of long-term isolation from other areas, as well as a population bottleneck due to retraction from LGM distribution into current range sizes. The still sparsely available phylogeographic studies support

these predictions, suggesting isolated lineages of frogs, birds and mammals in these enclaves showing recent demographic reduction (Carnaval and Bates, 2007; Tchaika et al., 2007; Cabanne et al., 2008; d'Horta et al., 2011; see Table 1). Another supporting biological evidence on the long-term isolation of the North Ceará enclaves comes from a dated phylogeny of the gnateaters (Aves: Conopophagidae) that shows the northern AF bird Conopophaga cearae with divergent populations between BN and CD, during the Quaternary (Batalha-Filho et al., 2014). We suggest that the high degree of isolation seen in North Ceará enclaves across the last glacial cycle modeled here (with cycle extremes expressed in MH, LGM, and LIG) might have been consistent in most glacial cycles that came before, which are estimated to show the same intensity and duration. Finally, the isolated Chapada Diamantina forest enclaves below the São Francisco River exhibited an alternative, distinct historical scenario involving high connectivity with coastal forests throughout all modeled periods. Although the Chapada Diamantina enclaves are currently 73

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5. Conclusions

– No demographic pattern assessed Yes

– No demographic pattern assessed Yes

No (but see text) Demographic stability

isolated within the Caatinga seasonally dry forest and woodlands, their long-term, constant connection with coastal rainforests suggests that they share closely related populations. These enclaves were reduced during MH and expanded very recently into its current range size (Fig. 2B), suggesting that a signature of recent expansion should be expected in these populations. Phylogeographic studies with birds that have sampled Chapada Diamantina populations often show weak genetic structure with respect to coastal AF populations (e.g., Cabanne et al., 2008; Maldonado-Coelho, 2012; Amaral et al., 2013; Cabanne et al., 2013). Population expansion, however, was not detected in these studies, and this might be related to high connectivity levels. If populations in this area are indeed highly connected to those in coastal AF, expansion of forests in the Chapada Diamantina enclaves would leave a signature of demographic expansion on the population edge, seen in the genetic pattern of the total population.

Here, we depicted the evolutionary history of the northern AF in the last 127 kyr. The paleoclimatic modeling has revealed new insights into the late Pleistocene biogeographic dynamics of rainforest enclaves that are currently isolated within the Brazilian Caatinga seasonally dry woodlands. Understanding of local historical diversification processes in such interesting island-like systems has been, however, largely overlooked within the context of the extraordinarily rich Atlantic Forest. Our models strongly support two main conclusions: (i) expansion of currently isolated forest patches during the LGM, which is unpredicted by classical refuge hypothesis; and (ii) different phylogeographic histories in those forest enclaves throughout the late Pleistocene. Idiosyncratic phylogeographic scenarios may also be predicted for each region (Fig. 3): (i) populations in Pernambuco/Paraíba and Araripe enclaves will show signatures of gene flow with coastal populations in the north of the São Francisco River, as well as signs of recent population size reduction; (ii) populations in North Ceará enclaves will also show signs of recent population size reduction, but deeper genetic isolation from all other northern AF forest islands (with high phylogeographic, and potentially high species endemism), as well as low levels of intrapopulational genetic diversity (based on smaller range sizes and the strong effect of drift in isolated populations); and (iii) populations in Chapada Diamantina enclaves will exhibit recent demographic expansion, low genetic diversity, and high levels of gene flow with coastal forests populations in the south of the São Francisco River. These biogeographic hypotheses are helpful to guide further studies and, hence, to advance our understanding of the evolutionary history of the AF biodiversity. Each of these historical scenarios can be rigorously tested by Approximate Bayesian Computation (ABC) approach (Knowles, 2009), which is currently largely used as a framework for hypothesis testing in AF phylogeography (e.g., Carnaval et al., 2009; Batalha-Filho et al., 2012; Amaral et al., 2013; Cabanne et al., 2013; Thomé et al., 2014; Brunes et al., 2015). Comparative phylogeographic approach should also be used whenever possible, especially due to among-species ecological differences in explaining phylogeographic patterns (Papadopoulou and Knowles, 2016). To optimally leverage the promising ABC approach in tests of historical scenarios, such development should go hand-in-hand with the proposed hypotheses in comparative phylogeographic studies that comprehensively sample the biodiversity across the ecologically and historically dynamic rainforest enclaves. Acknowledgments

Batalha-Filho et al. (2014)

Cabanne et al. (2013)

Maldonado-Coelho (2012) Amaral et al. (2013)

d'Horta et al. (2011)

Cabanne et al. (2008)

High Fst levels (0.6–0.7 kyr) between northern enclaves populations and other areas Divergent lineages north of the São Francisco River, which diverged during the late Pleistocene (100–400 kyr) No structure between Chapada Diamantina enclave and coastal Atlantic Forest Lineage in northern enclaves that diverged during the late Pleistocene (100–400 kyr) No structure between Chapada Diamantina enclave and coastal Atlantic Forest Low structure level between Chapada Diamantina enclave and coastal Atlantic Forest No genetic structure between Chapada Diamantina enclave and coastal Atlantic Forest Divergent species occurring north of São Francisco River

Yes (but see text about old divergence) Yes

Yes

No (but see text)

Yes

Yes (North Ceará enclaves populations) No (Chapada Diamantina populations, but see text)

Demographic reduction in northern enclaves populations; Demographic stability in Chapada Diamantina enclaves populations Demographic reduction in northern enclaves populations Demographic stability Yes (but see text about old divergence)

No (but the population expansion is dated to forest expansion periods as predicted by speleothem data) – Demographic expansion in northeastern enclaves No demographic pattern assessed Yes (but see text about old divergence) Yes Divergent lineages in northern enclaves before the Pleistocene

Carnaval and Bates (2007) Tchaika et al. (2007)

Genetic pattern Genetic pattern

Match the model

Demography Genetic structure Reference

Table 1 Phylogeographic studies in which genetic sampling encompassed the rainforest enclaves of the northern Atlantic Forest in the Brazilian Northeast.

Match the model

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M.H.B·S acknowledges the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for doctoral fellowship. H.B·F thanks the financial support from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 443249/2014-8 and 307037/2018-5), 74

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PROPCI/UFBA (PRODOC-2013/5813) and Fundação de Amparo à Pesquisa do Estado da Bahia – FAPESB (RED0045/2014 and JCB0026/ 2016). D.C. and H.B.F. also acknowledge the CNPq Research Productivity Fellowships (308244/2018-4 and 307037/2018-5, respectively). D.C. thanks Prêmio CAPES de Teses (23038.009148/201319), FAPESB (APP0037/2016), and Newton Advanced Fellowship (NAF \R1\180331) for supporting financially his research on plant biodiversity. We thank the four anonymous reviewers for their constructive comments that improved the manuscript.

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