Discovery of cryptic plant diversity on the rooftops of the Alps.

High elevation temperate mountains have long been considered species poor owing to high extinction or low speciation rates during the Pleistocene. We performed a phylogenetic and population genomic investigation of an emblematic high-elevation plant clade (Androsace sect. Aretia, 31 currently recognized species), based on plant surveys conducted during alpinism expeditions. We inferred that this clade originated in the Miocene and continued diversifying through Pleistocene glaciations, and discovered three novel species of Androsace dwelling on different bedrock types on the rooftops of the Alps. This highlights that temperate high mountains have been cradles of plant diversity even during the Pleistocene, with in-situ speciation driven by the combined action of geography and geology. Our findings have an unexpected historical relevance: H.-B. de Saussure likely observed one of these species during his 1788 expedition to the Mont Blanc and we describe it here, over two hundred years after its first sighting.

Diversification rate vs. diversification density: Decoupled consequences of plant height for diversification of Alooideae in time and space.

While biodiversity hotspots are typically identified on the basis of species number per unit area, their exceptional richness is often attributed, either implicitly or explicitly, to high diversification rates. High species concentrations, however, need not reflect rapid diversification, with the diversity of some hotspots accumulating at modest rates over long timespans. Here we explore the relationship between diversification in time vs. diversification in space and develop the concept of diversification density to describe the spatial scale of species accumulation in a clade. We investigate how plant height is associated with both aspects of diversification in Alooideae, a large plant subfamily with its center of diversity in the Greater Cape Floristic Region. We first reconstruct a time-calibrated phylogeny for Alooideae and demonstrate an evolutionary tendency towards reduced plant height. While plant height does not correlate with diversification rate across Alooideae it does so with diversification per unit space: clades of small plants tend to have the highest diversification densities. Furthermore, we find that diversification in time vs. space are uncorrelated. Our results show that diversification rate and density can be decoupled, and suggest that while some biodiversity hotspots might have been generated by high diversification rates, others are the product of high diversification density.

Species Selection Regime and Phylogenetic Tree Shape.

Species selection, the effect of heritable traits in generating between-lineage diversification rate differences, provides a valuable conceptual framework for understanding the relationship between traits, diversification, and phylogenetic tree shape. An important challenge, however, is that the nature of real diversification landscapes-curves or surfaces which describe the propensity of species-level lineages to diversify as a function of one or more traits-remains poorly understood. Here, we present a novel, time-stratified extension of the QuaSSE model in which speciation/extinction rate is specified as a static or temporally shifting Gaussian or skewed-Gaussian function of the diversification trait. We then use simulations to show that the generally imbalanced nature of real phylogenetic trees, as well as their generally greater than expected frequency of deep branching events, are typical outcomes when diversification is treated as a dynamic, trait-dependent process. Focusing on four basic models (Gaussian-speciation with and without background extinction; skewed-speciation; Gaussian-extinction), we also show that particular features of the species selection regime produce distinct tree shape signatures and that, consequently, a combination of tree shape metrics has the potential to reveal the species selection regime under which a particular lineage diversified. We evaluate this idea empirically by comparing the phylogenetic trees of plant lineages diversifying within climatically and geologically stable environments of the Greater Cape Floristic Region, with those of lineages diversifying in environments that have experienced major change through the Late Miocene-Pliocene. Consistent with our expectations, the trees of lineages diversifying in a dynamic context are less balanced, show a greater concentration of branching events close to the present, and display stronger diversification rate-trait correlations. We suggest that species selection plays an important role in shaping phylogenetic trees but recognize the need for an explicit probabilistic framework within which to assess the likelihoods of alternative diversification scenarios as explanations of a particular tree shape. [Cape flora; diversification landscape; environmental change; gamma statistic; species selection; time-stratified QuaSSE model; trait-dependent diversification; tree imbalance.].

A General Model for Estimating Macroevolutionary Landscapes.

The evolution of quantitative characters over long timescales is often studied using stochastic diffusion models. The current toolbox available to students of macroevolution is however limited to two main models: Brownian motion and the Ornstein-Uhlenbeck process, plus some of their extensions. Here, we present a very general model for inferring the dynamics of quantitative characters evolving under both random diffusion and deterministic forces of any possible shape and strength, which can accommodate interesting evolutionary scenarios like directional trends, disruptive selection, or macroevolutionary landscapes with multiple peaks. This model is based on a general partial differential equation widely used in statistical mechanics: the Fokker-Planck equation, also known in population genetics as the Kolmogorov forward equation. We thus call the model FPK, for Fokker-Planck-Kolmogorov. We first explain how this model can be used to describe macroevolutionary landscapes over which quantitative traits evolve and, more importantly, we detail how it can be fitted to empirical data. Using simulations, we show that the model has good behavior both in terms of discrimination from alternative models and in terms of parameter inference. We provide R code to fit the model to empirical data using either maximum-likelihood or Bayesian estimation, and illustrate the use of this code with two empirical examples of body mass evolution in mammals. FPK should greatly expand the set of macroevolutionary scenarios that can be studied since it opens the way to estimating macroevolutionary landscapes of any conceivable shape. [Adaptation; bounds; diffusion; FPK model; macroevolution; maximum-likelihood estimation; MCMC methods; phylogenetic comparative data; selection.].

Plant size: a key determinant of diversification?

Explaining the variation in diversification rate across groups of plants has long been an important goal of botanists. In plants, complex scenarios involving a combination of extrinsic opportunities and intrinsic traits have been used to explain rapid diversification in certain groups. However, we feel that a very simple trait has been neglected from theories of plant diversification, namely plant height. Here, we argue that decreasing plant size should generally lead to an increase in speciation rate and a decrease in extinction rate. Theory suggests that all population genetic processes involved in speciation are influenced by plant size and its correlates, including seed dispersal distance, population size, generation time and the spatial scale at which plants perceive environmental heterogeneity. In addition, several of these variables, notably population size, also influence rates of extinction. We support our arguments with an empirical analysis showing that plant height is indeed negatively correlated with net diversification rate across families of angiosperms. Finally, we outline how the finer aspects of our hypothesis could be tested, at both micro- and macroevolutionary scales. In addition to strengthening our understanding of the effect of plant size on evolutionary processes, such a research agenda should contribute novel insights to speciation theory in general.

How Do Cold-Adapted Plants Respond to Climatic Cycles? Interglacial Expansion Explains Current Distribution and Genomic Diversity in Primula farinosa L.

Understanding the effects of past climatic fluctuations on the distribution and population-size dynamics of cold-adapted species is essential for predicting their responses to ongoing global climate change. In spite of the heterogeneity of cold-adapted species, two main contrasting hypotheses have been proposed to explain their responses to Late Quaternary glacial cycles, namely, the interglacial contraction versus the interglacial expansion hypotheses. Here, we use the cold-adapted plant Primula farinosa to test two demographic models under each of the two alternative hypotheses and a fifth, null model. We first approximate the time and extent of demographic contractions and expansions during the Late Quaternary by projecting species distribution models across the last 72 ka. We also generate genome-wide sequence data using a Reduced Representation Library approach to reconstruct the spatial structure, genetic diversity, and phylogenetic relationships of lineages within P. farinosa. Finally, by integrating the results of climatic and genomic analyses in an Approximate Bayesian Computation framework, we propose the most likely model for the extent and direction of population-size changes in $P$. farinosa through the Late Quaternary. Our results support the interglacial expansion of $P$. farinosa, differing from the prevailing paradigm that the observed distribution of cold-adapted species currently fragmented in high altitude and latitude regions reflects the consequences of postglacial contraction processes.

Do floral and niche shifts favour the establishment and persistence of newly arisen polyploids? A case study in an Alpine primrose.

BACKGROUND AND AIMS: Polyploidization plays a key role in plant evolution. Despite the generally accepted 'minority-cytotype exclusion' theory, the specific mechanisms leading to successful establishment and persistence of new polyploids remain controversial. The majority of newly formed polyploids do not become established, because they are less common, have fewer potential mates or may not be able to compete successfully with co-occurring progenitors at lower ploidy levels. Changes in floral traits and ecological niches have been proposed as important mechanisms to overcome this initial frequency-dependent disadvantage. The aim of this study was to determine whether dodecaploids of the heterostylous P. marginata differ from their hexaploid progenitors in P. marginata and P. allionii for selected floral traits and ecological preferences that might be involved in establishment and persistence, providing a possible explanation for the origin of polyploidized populations. METHODS: Floral morphological traits and ecological niche preferences among dodecaploids and their hexaploid progenitors in P. marginata and P. allionii ,: all restricted to the south-western Alps, were quantified and compared KEY RESULTS: Differences in floral traits were detected between dodecaploids and their closest relatives, but such differences might be too weak to counter the strength of minority cytotype disadvantage and are unlikely to enable the coexistence of different cytotypes. Furthermore, the results suggest the preservation of full distyly and no transition to selfing in dodecaploids. Finally, dodecaploids occur almost exclusively in environments that are predicted to be suitable also for their closest hexaploid relatives. CONCLUSIONS: In light of the results, P. marginata dodecaploids have probably been able to establish and persist by occupying geographical areas not yet filled by their closest relatives without significant evolution in their climatic and pollination niches. Dispersal limitation and minority-cytotype exclusion probably maintain their current range disjunct from those of its close relatives.

Inferring Bounded Evolution in Phenotypic Characters from Phylogenetic Comparative Data.

Our understanding of phenotypic evolution over macroevolutionary timescales largely relies on the use of stochastic models for the evolution of continuous traits over phylogenies. The two most widely used models, Brownian motion and the Ornstein-Uhlenbeck (OU) process, differ in that the latter includes constraints on the variance that a trait can attain in a clade. The OU model explicitly models adaptive evolution toward a trait optimum and has thus been widely used to demonstrate the existence of stabilizing selection on a trait. Here we introduce a new model for the evolution of continuous characters on phylogenies: Brownian motion between two reflective bounds, or Bounded Brownian Motion (BBM). This process also models evolutionary constraints, but of a very different kind. We provide analytical expressions for the likelihood of BBM and present a method to calculate the likelihood numerically, as well as the associated R code. Numerical simulations show that BBM achieves good performance: parameter estimation is generally accurate but more importantly BBM can be very easily discriminated from both BM and OU. We then analyze climatic niche evolution in diprotodonts and find that BBM best fits this empirical data set, suggesting that the climatic niches of diprotodonts are bounded by the climate available in Australia and the neighboring islands but probably evolved with little additional constraints. We conclude that BBM is a valuable addition to the macroevolutionary toolbox, which should enable researchers to elucidate whether the phenotypic traits they study are evolving under hard constraints between bounds.

Does the legacy of historical biogeography shape current invasiveness in pines?

Why are some introduced species more successful at establishing and spreading than others? Until now, characteristics of extant species have been intensively investigated to answer this question. We propose to gain new insights on species invasiveness by exploring the long-term biogeographic and evolutionary history of lineages. We exemplify our approach using one of the best-studied invasive plant genera, Pinus. We notably estimated the historical biogeography of pines and the rates of trait evolution in pines. These estimates were analysed with regard to species invasiveness status. The results revealed that currently invasive species belong to lineages that were particularly successful at colonizing new regions in the past. We also showed that highly mobile lineages had faster rates of niche evolution, but that these rates are poor proxies for species adaptive potential in invaded regions (estimated by niche shift among native and invaded regions). In summary, working at the interface of ecology, historical biogeography and evolutionary history offers stimulating perspectives to improve our understanding of the drivers of invasion success.

Phylogenetic niche conservatism - common pitfalls and ways forward.

1. The prevalence of phylogenetic niche conservatism (PNC) in nature is still a conflicting issue. Disagreement arises from confusion over its precise definition and the variety of approaches to measure its prevalence. Recent work highlighted that common measures of PNC strongly depend on the assumptions of the underlying model of niche evolution. However, this warning has not been well recognized in the applied literature and questionable approaches are still frequently applied. 2. The aim of this paper is to draw attention to the assumptions underlying commonly applied simple measures of PNC. We used a series of simulations to illustrate how misleading results can be if assumptions of niche evolution are violated, that the violation of assumptions is a common phenomenon and that testing assumptions requires in-depth pre-test. 3. We conclude that the seemingly simple measures of PNC, such as phylogenetic sign6al and evolutionary rate, are not so easy to apply if one accounts for the necessity to test model assumptions. In addition, these measures can be difficult to interpret. The common assumption that strong phylogenetic signal indicates PNC will be often invalid. In addition, the interpretation of some measures, e.g. the conclusion that evolutionary rate is slow enough to indicate PNC, requires a comparison with another clade, another trait or well-developed null model assumptions and thus additional data. 4. We suggest that studies investigating PNC should always compare alternative evolutionary models, and that model comparisons should in particular include flexible niche evolution models such as multiple-optima OU models, although these are computational intensive. These models are directly inherited from the concept of macro-evolutionary adaptive landscape, and can indicate PNC either by relative few peak shifts or by narrow peaks in the adaptive landscape. A test of PNC thus requires comparing these parameters of the macroevolutionary landscape between clades or time periods. 5. The general prevalence of PNC in nature should be evaluated only based on studies keeping up to the high standards of communicating the used definition of PNC, testing the assumptions made in the modelling approaches and including newly developed models in a model comparison approach.

Neutral biogeography and the evolution of climatic niches.

Recent debate on whether climatic niches are conserved through time has focused on how phylogenetic niche conservatism can be measured by deviations from a Brownian motion model of evolutionary change. However, there has been no evaluation of this methodological approach. In particular, the fact that climatic niches are usually obtained from distribution data and are thus heavily influenced by biogeographic factors has largely been overlooked. Our main objective here was to test whether patterns of climatic niche evolution that are frequently observed might arise from neutral dynamics rather than from adaptive scenarios. We developed a model inspired by neutral biodiversity theory, where individuals disperse, compete, and undergo speciation independently of climate. We then sampled the climatic niches of species according to their geographic position and showed that even when species evolve independently of climate, their niches can nonetheless exhibit evolutionary patterns strongly differing from Brownian motion. Indeed, climatic niche evolution is better captured by a model of punctuated evolution with constraints due to landscape boundaries, two features that are traditionally interpreted as evidence for selective processes acting on the niche. We therefore suggest that deviation from Brownian motion alone should not be used as evidence for phylogenetic niche conservatism but that information on phenotypic traits directly linked to physiology is required to demonstrate that climatic niches have been conserved through time.

Unravelling the architecture of functional variability in wild populations of Polygonum viviparum L.

Functional variability (FV) of populations can be decomposed into three main features: the individual variability of multiple traits, the strength of correlations between those traits and the main direction of these correlations, the latter two being known as 'phenotypic integration'. Evolutionary biology has long recognized that FV in natural populations is key to determining potential evolutionary responses, but this topic has been little studied in functional ecology.Here we focus on the arctico-alpine perennial plant species Polygonum viviparum L.. We used a comprehensive sampling of seven functional traits in 29 wild populations covering the whole environmental niche of the species. The niche of the species was captured by a temperature gradient, which separated alpine stressful habitats from species-rich, competitive sub-alpine ones. We seeked to assess the relative roles of abiotic stress and biotic interactions in shaping different aspects of functional variation within and among populations, that is, the multi-trait variability, the strength of correlations between traits, and the main directions of functional trade-offs.Populations with the highest extent of functional variability were found in the warm end of the gradient whereas populations exhibiting the strongest degree of phenotypic integration were located in sites with intermediate temperatures. This could reveal both the importance of environmental filtering and population demography in structuring FV. Interestingly, we found that the main axes of multivariate functional variation were radically different within and across population.Although the proximate causes of FV structure remain uncertain, our study presents a robust methodology for the quantitative study of functional variability in connection with species' niches. It also opens up new perspectives for the conceptual merging of intraspecific functional patterns with community ecology.

Replicated radiations of the alpine genus Androsace (Primulaceae) driven by range expansion and convergent key innovations.

AIM: We still have limited understanding of the contingent and deterministic factors that have fostered the evolutionary success of some species lineages over others. We investigated how the interplay of intercontinental migration and key innovations promoted diversification of the genus Androsace. LOCATION: Mountain ranges and cold steppes of the Northern Hemisphere. METHODS: We reconstructed ancestral biogeographical ranges at regional and continental scales by means of a dispersal-extinction-cladogenesis analysis using dated Bayesian phylogenies and contrasting two migration scenarios. Based on diversification analyses under two frameworks, we tested the influence of life form on speciation rates and whether diversification has been diversity-dependent. RESULTS: We found that three radiations occurred in this genus, at different periods and on different continents, and that life form played a critical role in the history of Androsace. Short-lived ancestors first facilitated the expansion of the genus' range from Asia to Europe, while cushions, which appeared independently in Asia and Europe, enhanced species diversification in alpine regions. One long-distance dispersal event from Europe to North America led to the diversification of the nested genus Douglasia. We found support for a model in which speciation of the North American-European clade is diversity-dependent and close to its carrying capacity, and that the diversification dynamics of the North American subclade are uncoupled from this and follow a pure birth process. MAIN CONCLUSIONS: The contingency of past biogeographical connections combined with the evolutionary determinism of convergent key innovations may have led to replicated radiations of Androsace in three mountain regions of the world. The repeated emergence of the cushion life form was a convergent key innovation that fostered radiation into alpine habitats. Given the large ecological similarity of Androsace species, allopatry may have been the main mode of speciation.

Reconstructing the origins of high-alpine niches and cushion life form in the genus Androsace S.L. (Primulaceae).

Relatively, few species have been able to colonize extremely cold alpine environments. We investigate the role played by the cushion life form in the evolution of climatic niches in the plant genus Androsace s.l., which spreads across the mountain ranges of the Northern Hemisphere. Using robust methods that account for phylogenetic uncertainty, intraspecific variability of climatic requirements and different life-history evolution scenarios, we show that climatic niches of Androsace s.l. exhibit low phylogenetic signal and that they evolved relatively recently and punctually. Models of niche evolution fitted onto phylogenies show that the cushion life form has been a key innovation providing the opportunity to occupy extremely cold environments, thus contributing to rapid climatic niche diversification in the genus Androsace s.l. We then propose a plausible scenario for the adaptation of plants to alpine habitats.