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This article was submitted to Evolutionary and Population Genetics, a section of the journal Frontiers in Genetics.
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Tropical rain forests (TRF) are the most diverse terrestrial biome on Earth, but the diversification dynamics of their constituent growth forms remain largely unexplored. Climbing plants contribute significantly to species diversity and ecosystem processes in TRF. We investigate the broad-scale patterns and drivers of species richness as well as the diversification history of climbing and non-climbing palms (Arecaceae). We quantify to what extent macroecological diversity patterns are related to contemporary climate, forest canopy height, and paleoclimatic changes. We test whether diversification rates are higher for climbing than non-climbing palms and estimate the origin of the climbing habit. Climbers account for 22% of global palm species diversity, mostly concentrated in Southeast Asia. Global variation in climbing palm species richness can be partly explained by past and present-day climate and rain forest canopy height, but regional differences in residual species richness after accounting for current and past differences in environment suggest a strong role of historical contingencies in climbing palm diversification. Climbing palms show a higher net diversification rate than non-climbers. Diversification analyses of palms detected a diversification rate increase along the branches leading to the most species-rich clade of climbers. Ancestral character reconstructions revealed that the climbing habit originated between early Eocene and Miocene. These results imply that changes from non-climbing to climbing habits may have played an important role in palm diversification, resulting in the origin of one fifth of all palm species. We suggest that, in addition to current climate and paleoclimatic changes after the late Neogene, present-day diversity of climbing palms can be explained by morpho-anatomical innovations, the biogeographic history of Southeast Asia, and/or ecological opportunities due to the diversification of high-stature dipterocarps in Asian TRFs.
“The object of all climbing plants is to reach the light and free air with as little expenditure of organic matter as possible.”
Besides being the most diverse terrestrial ecosystem on Earth, tropical rain forests (TRF) contain a wide array of growth forms such as large emergent to small understory trees, shrubs, epiphytes, lianas, and vines, as well as parasitic plants (
The climbing growth form (lianas and vines) constitutes a key component of tropical forests worldwide, contributing considerably to species diversity (between 10–50%), stem density (∼25%), and ecosystem processes such as forest transpiration and carbon sequestration (
Despite their ecological importance, few studies have investigated the role of the climbing habit in the evolution and diversification of TRF. Based on sister group comparisons of species richness between climbing and non-climbing clades within 48 angiosperm families,
With about 2,500 species, palms (Arecaceae) are a species-rich, monocotyledonous plant family characteristic of tropical and subtropical ecosystems (
A large diversity of growth forms has evolved within palms, including tree palms, palms with clustered stems, acaulescent palms, and climbing palms (
Species diversity of climbers within palm genera.
Genus (# spp./total #) | % climber | Subfamily | Regional distribution |
---|---|---|---|
91 | Calamoideae | Afrotropics, Indomalaya, Australasia, Oceania | |
100 | Calamoideae | Indomalaya | |
0.01 | Arecoideae | Neotropics | |
90 | Calamoideae | Indomalaya, Australasia | |
100 | Arecoideae | Neotropics | |
0.01 | Arecoideae | Afrotropics (Madagascar) | |
100 | Calamoideae | Afrotropics | |
100 | Calamoideae | Indomalaya, Australasia | |
100 | Calamoideae | Afrotropics | |
100 | Calamoideae | Indomalaya | |
100 | Calamoideae | Afrotropics | |
100 | Calamoideae | Indomalaya | |
100 | Calamoideae | Indomalaya | |
67 | Calamoideae | Indomalaya | |
100 | Calamoideae | Indomalaya | |
As in most other monocotyledons, palms lack a vascular cambium for secondary growth. Instead, they retain their primary anatomical architecture of the stem for their entire life. Nevertheless, they can still achieve remarkable heights of up to 60 m tall (
Here, we combine macroecological and macroevolutionary analyses to investigate the role of climbing in the evolutionary history of palms. We quantify global patterns and drivers of climbing palm diversity and ask what role the climbing habit has played in the diversification of palms through time. Specifically, we test the following hypotheses and corresponding predictions:
The diversity of climbing palms correlates with aseasonal tropical climates and peaks in high-stature forests:
(a) Due to physiological and functional adaptations of palms, species richness of climbing palms is positively correlated with temperature and precipitation and negatively with temperature seasonality.
(b) Differences in canopy height among TRFs explain global variation in species richness of climbing palms, with tall forests having more climbing species than short-stature forests.
The climbing habit has played an important role in palm diversification:
(a) Diversification rates are higher for climbing than non-climbing palms lineages.
(b) The origin of the climbing habit correlates with increases in diversification rates.
We used data on global palm species distributions from an exhaustive, authoritative checklist of the World’s palm species (
The dataset contained a total of 2,445 accepted palm species names and 5,027 native occurrence records within 194 TDWG level 3 units (
We classified all palm species into two growth forms: (1) climbers, and (2) non-climbers (including all other growth forms such as stemmed and acaulescent palms). Palm species that show leaning growth forms such as some
We tested 14 predictor variables as potential determinants of species richness in climbing and non-climbing palms. These variables reflected contemporary climate (six variables), paleoclimate (six variables), canopy height (one variable), and biogeographic region (one variable). Present and past climates (
To represent contemporary climate, we chose six climatic predictor variables from the Worldclim dataset (version 1.4;
To represent paleoclimatic changes over the Neogene and Quaternary epochs, we compiled both temperature and precipitation data from paleoclimatic reconstructions representing the Last Glacial Maximum (LGM, ca. 21,000 years ago), the late Pliocene (∼3 mya), and the late Miocene (∼10 mya). Data for the LGM were compiled from two climate simulations representing the Community Climate System Model version 3 (CCSM3) and the Model for Interdisciplinary Research on Climate version 3.2 (MIROC3.2), both of which were part of the second phase of the Paleoclimate Modeling Intercomparison Project
We included canopy height (CANOPY) of tropical rain forests as a predictor variable to test whether species richness of climbing palms increases with the tallness of forests. Forest canopy height data were derived from a recent global map of forest heights (
We derived a biogeographic variable (REGION) to capture potential effects related to the long-term history of biogeographic regions. This categorical variable distinguished seven major regions: Afrotropics, Australasia, Indomalaya, Nearctic, Neotropics, Oceania, and Palaearctic (
We assessed the environmental determinants of species richness of both climbers and non-climbers with separate multi-predictor regression models. We only included TDWG level 3 units where species richness >0 and for which environmental data were available. A number of smaller islands had to be excluded for non-climbing palms because canopy height data were not available for those. Hence, final sample sizes for the statistical analysis were 82 and 164 TDWG level 3 units for climbers and non-climbers, respectively.
We used generalized linear models (GLM) with a Gaussian error distribution and included all 14 predictor variables as well as either species richness of climbers or non-climbers as response variable. We then applied a model selection based on the Akaike Information Criterion (AIC) to derive a minimum adequate model that had the smallest possible number of predictor variables (i.e., the lowest AIC value;
To test for a potential influence of spatial autocorrelation (
Beyond examining the determinants of species richness of climbers and non-climbers, we performed diversification analyses to test whether the evolution of climbers has an impact on diversification rates as a whole and for specific clades.
We used the Cladogenetic State Speciation and Extinction model (ClaSSE,
Different proportions of climbers and non-climbers within genera (see
The 100 trees generated above were combined with the trait dataset of growth forms. The ClaSSE model is a derived model of the binary state speciation and extinction model (BiSSE) (
To identify the best model given our data we considered ten ClaSSE diversification scenarios (
Null model (three free parameters): diversification rates are independent of growth form (λ111 = λ000 = λ110 = λ001 = λ100 = λ011, μ1 = μ0, and q10= q01),
Cladogenetic speciation model (eight free parameters): growth form only affects cladogenetic speciation (λ111 ≠ λ000 ≠ λ110 ≠ λ001 ≠ λ100 ≠ λ011, μ1= μ0, and q10= q01),
Symmetrical cladogenetic speciation model (five free parameters): growth form only affects symmetrical cladogenetic speciation (λ111 ≠ λ000, λ110 = λ001 = λ100 = λ011, μ1= μ0, and q10= q01),
Asymmetrical cladogenetic speciation model (seven free parameters): growth form only affects asymmetrical cladogenetic speciation (λ111 = λ000, λ110 ≠ λ001 ≠ λ100 ≠ λ011, μ1= μ0, and q10= q01),
Anagenetic state change model (four free parameters): growth form only affects anagenetic state change (λ111 = λ000 = λ110 = λ001 = λ100 = λ011, μ1 = μ0, and q10 ≠ q01),
Extinction model (four free parameters): growth form only affects the extinction rate (λ111 = λ000 = λ110 = λ001 = λ100 =λ011, μ1 ≠ μ0, and q10= q01),
Cladogenetic speciation and extinction model (nine free parameters): growth form affects cladogenetic speciation and extinction (λ111 ≠ λ000 ≠ λ110 ≠ λ001 ≠ λ100 ≠ λ011, μ1 ≠ μ0, and q10= q01),
Anagenetic state change and extinction model (five free parameters): growth form affects anagenetic state change and extinction (λ111 = λ000 = λ110 = λ001 = λ100 = λ011, μ1 ≠ μ0, and q10 ≠ q01),
Cladogenetic and anagenetic state change model (nine free parameters): growth form affects both cladogenetic speciation and anagenetic state change (λ111 ≠ λ000 ≠ λ110 ≠ λ001 ≠ λ100 ≠ λ011, μ1= μ0, and q10 ≠ q01),
Full model (10 free parameters): components of the diversification rate are dependent on the growth form (λ111 ≠ λ000 ≠ λ110 ≠ λ001 ≠ λ100 ≠ λ011, μ1 ≠ μ0, and q10 ≠ q01).
All analyses on both datasets were performed using the R-package
In order to test for possible shifts in diversification rates (speciation minus extinction) associated with the evolution of the climbing habit we used the Bayesian Analysis of Macroevolutionary Mixtures approach implemented in BAMM version 2.2.0 (
The main assumption of previous methods for identifying diversification rate shifts in phylogenies was based on constant rates between the shifts (e.g., MEDUSA,
BAMM accommodates incomplete taxon sampling under a phylogenetically structured sampling. In our phylogeny, we have included most palm genera, each one being represented by a single species. We thus provided BAMM with the proportion of species sampled per genus (i.e., 1/number of species in genus). We used the chronogram of palm genera as the input tree (
Post run analyses were undertaken in BAMMTools following
In contrast to methods that identify a single best rate shift configuration across a tree (e.g., MEDUSA), BAMM identifies a set of most credible rate shift sets (CSS) ordering them by posterior probability (
Finally, we scaled the phylogenetic tree to be proportional to the BF and marginal probabilities of a rate shift along a branch. This helps to visualizes the topological location of diversification rate shifts.
To identify how many times and when the climbing habit arose in palms above the genus level, we conducted an ancestral character reconstruction using a stochastic character (posterior) mapping approach, as implemented in the program SIMMAP (
Out of 2,446 palm species in our dataset, a total of 535 species (22%) were classified as climbers. The majority of climbing palm species are found within the genera
Among contemporary climatic variables, TEMP (positive effect) and PREC SEAS (negative effect) were the most important variables to explain climber species richness in the minimum adequate models (
Multiple-predictor regression models to explain global species richness of climbing (
Palm species richness |
||||||
---|---|---|---|---|---|---|
Climbers |
Non-climbers |
|||||
Standard coefficient | Standard coefficient | |||||
Intercept | 2.798 | *** | 2.413 | *** | ||
CANOPY | ** | * | ||||
CANOPY2 | NA | 0.063 | n.s. | |||
PREC | 0.271 | n.s. | ||||
TEMP | *** | *** | ||||
PREC SEAS | * | 0.219 | n.s. | |||
PREC SEAS2 | NA | 0.044 | n.s. | |||
TEMP SEAS | ** | |||||
TEMP SEAS2 | NA | |||||
PREC DRY | NA | |||||
PREC DRY2 | NA | NA | ||||
TEMP COLD | NA | |||||
TEMP COLD2 | NA | |||||
LGMPREC | ||||||
LGMPREC2 | NA | |||||
LGMTEMP | 0.220 | n.s. | ||||
PLIOPREC | * | n.s. | ||||
PLIOPREC2 | NA | * | ||||
PLIOTEMP | ||||||
MIOPREC | n.s. | n.s. | ||||
MIOPREC2 | NA | * | ||||
MIOTEMP | ||||||
REGION | ||||||
Afrotropics | *** | *** | ||||
Australasia | *** | 0.078 | n.s. | |||
Neotropics | *** | 0.658 | n.s. | |||
Oceania | NA | n.s. | ||||
Nearctic | NA | n.s. | ||||
Palearctic | NA | * | ||||
200 | 443 | |||||
0.69 | 0.70 | |||||
Moran’s |
n.s. | 0.11 | n.s. |
The minimum adequate models included CANOPY as an important predictor variable for the species richness of both non-climbing and climbing palms, but the effect was stronger for climbers than for non-climbing palms (
Comparing the ten ClaSSE diversification models revealed that model 7, the cladogenetic speciation and extinction model, was the best fitting model based on average AICc values from the 100 trees (
Inferred rates of speciation and extinction for climbing and non-climbing palms using the Cladogenetic State Speciation and Extinction model (ClaSSE) for the best fitting model (model 7) out of ten (see
Model | df | logL | AICc | λ000 | λ001 | λ011 | λ100 | λ110 | λ111 | μ0 | μ1 | q01 = q10 |
---|---|---|---|---|---|---|---|---|---|---|---|---|
Model 7 (non-constrained) | 9 | -5582 | 11182 | 0,64 | 0,00004 | 0,00015 | 0,00021 | 0,00002 | 0,87 | 0,61 | 0,8 | 0,00002 |
SE | 0,011 | 0,00001 | 0,00001 | 0,00004 | 0,00001 | 0,094 | 0,012 | 0,097 | 0 | |||
Model 7 (constrained) | 9 | -5768 | 11554 | 0,53 | 0,00002 | 0,0002 | 0,00022 | 0,000001 | 0,58 | 0,485 | 0,491 | 0,00001 |
SE | 0,00504 | 0,000008 | 0,00001 | 0,00005 | 0,000001 | 0,022 | 0,005 | 0,025 | 0.000002 |
The BAMM analyses reached a stationary state well before 100,000 generations in all independent runs. The ESS values for the number of shifts and the log-likelihood were always above 200, indicating appropriate sampling of parameters from the posterior. Under the Poisson prior of 1.0, the zero rate shift model was rarely sampled from the posterior, strongly supporting the hypothesis of diversification rate heterogeneity across palms. Based on a Poisson prior of 0.1, the most probable number of rates shifts was 9 (PP = 0.135), closely followed by 8 (PP = 0.132), and 10 (PP = 0.131). This means that diversification rates have changed 9, 8, or 10 times across the history of palms.
The phylorate plot shows an increase in mean diversification rates at the crown node of subtribe Calaminae (depicted by an arrow in
The six most probable CSS’s (with a cumulative PP of 0.614,
Posterior mapping identified 4.9 average transformations from the non-climbing to the climbing state across the 100 trees, and 0.61 transformations in the opposite direction (reversals). These results do not include the three climbing species within the genera
Our results show that climbing palm species richness is associated with present-day climate (temperature, precipitation seasonality) and paleoclimatic changes since the late Neogene (Miocene and Pliocene;
Our results further support the hypothesis that climbing palms are more diverse in tall-stature forests than in lower canopy ones (
As indicated by
Evidence suggests that the evolution of climbers promoted diversification within angiosperms (
The analyses presented here suggest an important evolutionary role of climbers in explaining present-day palm diversity (hypothesis 2). Our ClaSSE analyses indicated that across palms, species with a climbing habit diversified on average 1.3 times faster when compared to species with a non-climbing habit (λ111 > λ000; see
Despite the overall higher diversification rate associated to climbers, the impact of the climbing trait on the diversification of specific clades is unclear (prediction 2a). Based on the analysis of the BAMM output, an increase in diversification rates (
The increase in diversification rates in Bactridinae does not appear to be related to the climbing habit that evolved in the genus
The ancestral state reconstructions indicated that the climbing habit evolved a minimum of five independent times in palms: four times in Calamoideae and once in Arecoideae (
Our results reveal an interesting pattern: the climbing habit appears to have had an impact on diversification rates in Calaminae, but not in other clades/genera where it evolved (Ancistrophyllinae, Plectocomiinae,
Explaining geographic differences in diversification rates (e.g., numerous climbing species in Southeast Asia vs. few in the Neotropics) might be related to the fact that a particular trait only increases diversification rates under certain environmental conditions (
One important and characteristic plant family in Southeast Asia is Dipterocarpaceae (
Global diversity patterns of climbing palms show a diversity anomaly relative to other palms, with a strong peak of species richness in Southeast Asian rain forests and low species richness in other regions (e.g., the Neotropics). Present-day climate, forest canopy heights, and paleoclimatic changes in the Neogene and Quaternary can partly explain this pattern, but they do not provide a sufficient explanation for the extraordinary diversification of climbing palms in Southeast Asia. An increase in diversification rates in Calaminae, even though not significant based on our data, relative to other climbers and non-climbers might instead be the outcome of anatomical and morphological innovations, the complex biogeographic history of Southeast Asia, and/or ecological opportunity responses to the regional presence and diversification of tall canopy trees such as dipterocarps. We suggest that, in addition to climatic and paleoclimatic factors, such historical and evolutionary contingencies play an important role in explaining present-day biodiversity across TRFs. New datasets (e.g., global high-quality species distribution data at fine resolutions, well resolved species-level phylogenies, and additional morphological trait data) as well as novel analytical tools will likely increase our knowledge of palm diversification and our understanding of tropical rain forest evolution in the future.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We thank John Dransfield for species-level information about climbing palms and Yanis Bouchenak-Khelladi for discussions and help with R scripts and diversification analyses. We are also grateful to two anonymous reviewers whose comments improved this manuscript. We thank James Richardson, Valenti Rull, and Toby Pennington for inviting us to submit our work to this special issue. W. Daniel Kissling acknowledges a University of Amsterdam (UvA) starting grant. Jens-Christian Svenning was supported by the European Research Council (ERC-2012-StG-310886-HISTFUNC) and the Danish Council for Independent Research | Natural Sciences (12-125079).