Exploring patterns of interspecific variation in quantitative traits using sequential phylogenetic eigenvector regressions

A number of metrics have been developed for estimating phylogenetic signal in data and to evaluate correlated evolution, inferring broad-scale evolutionary and ecological processes. Here, we proposed an approach called phylogenetic signal-representation (PSR) curve, built upon phylogenetic eigenvector regression (PVR). In PVR, selected eigenvectors extracted from a phylogenetic distance matrix are used to model interspecific variation. In the PSR curve, sequential PVR models are fitted after successively increasing the number of eigenvectors and plotting their R(2) against the accumulated eigenvalues. We used simulations to show that a linear PSR curve is expected under Brownian motion and that its shape changes under alternative evolutionary models. The PSR area, expressing deviations from Brownian motion, is strongly correlated (r= 0.873; P < 0.01) with Blomberg's K-statistics, so nonlinear PSR curves reveal if traits are evolving at a slower or higher rate than expected by Brownian motion. The PSR area is also correlated with phylogenetic half-life under an Ornstein-Uhlenbeck process, suggesting how both methods describe the shape of the relationship between interspecific variation and time since divergence among species. The PSR curve provides an elegant exploratory method to understand deviations from Brownian motion, in terms of acceleration or deceleration of evolutionary rates occurring at large or small phylogenetic distances.     

A phylogenetic analysis of macroevolutionary patterns in fermentative yeasts

When novel sources of ecological opportunity are available, physiological innovations can trigger adaptive radiations. This could be the case of yeasts (Saccharomycotina), in which an evolutionary novelty is represented by the capacity to exploit simple sugars from fruits (fermentation). During adaptive radiations, diversification and morphological evolution are predicted to slow‐down after early bursts of diversification. Here, we performed the first comparative phylogenetic analysis in yeasts, testing the “early burst” prediction on species diversification and also on traits of putative ecological relevance (cell‐size and fermentation versatility). We found that speciation rates are constant during the time‐range we considered (ca., 150 millions of years). Phylogenetic signal of both traits was significant (but lower for cell‐size), suggesting that lineages resemble each other in trait‐values. Disparity analysis suggested accelerated evolution (diversification in trait values above Brownian Motion expectations) in cell‐size. We also found a significant phylogenetic regression between cell‐size and fermentation versatility (R² = 0.10), which suggests correlated evolution between both traits. Overall, our results do not support the early burst prediction both in species and traits, but suggest a number of interesting evolutionary patterns, that warrant further exploration. For instance, we show that the Whole Genomic Duplication that affected a whole clade of yeasts, does not seems to have a statistically detectable phenotypic effect at our level of analysis. In this regard, further studies of fermentation under common‐garden conditions combined with comparative analyses are warranted.     

Rapid maximum likelihood ancestral state reconstruction of continuous characters: A rerooting‐free algorithm

Ancestral state reconstruction is a method used to study the evolutionary trajectories of quantitative characters on phylogenies. Although efficient methods for univariate ancestral state reconstruction under a Brownian motion model have been described for at least 25 years, to date no generalization has been described to allow more complex evolutionary models, such as multivariate trait evolution, non‐Brownian models, missing data, and within‐species variation. Furthermore, even for simple univariate Brownian motion models, most phylogenetic comparative R packages compute ancestral states via inefficient tree rerooting and full tree traversals at each tree node, making ancestral state reconstruction extremely time‐consuming for large phylogenies. Here, a computationally efficient method for fast maximum likelihood ancestral state reconstruction of continuous characters is described. The algorithm has linear complexity relative to the number of species and outperforms the fastest existing R implementations by several orders of magnitude. The described algorithm is capable of performing ancestral state reconstruction on a 1,000,000‐species phylogeny in fewer than 2 s using a standard laptop, whereas the next fastest R implementation would take several days to complete. The method is generalizable to more complex evolutionary models, such as phylogenetic regression, within‐species variation, non‐Brownian evolutionary models, and multivariate trait evolution. Because this method enables fast repeated computations on phylogenies of virtually any size, implementation of the described algorithm can drastically alleviate the computational burden of many otherwise prohibitively time‐consuming tasks requiring reconstruction of ancestral states, such as phylogenetic imputation of missing data, bootstrapping procedures, Expectation‐Maximization algorithms, and Bayesian estimation. The described ancestral state reconstruction algorithm is implemented in the Rphylopars functions anc.recon and phylopars.     

The best of both worlds: Phylogenetic eigenvector regression and mapping

Eigenfunction analyses have been widely used to model patterns of autocorrelation in time, space and phylogeny. In a phylogenetic context, Diniz-Filho et al. (1998) proposed what they called Phylogenetic Eigenvector Regression (PVR), in which pairwise phylogenetic distances among species are submitted to a Principal Coordinate Analysis, and eigenvectors are then used as explanatory variables in regression, correlation or ANOVAs. More recently, a new approach called Phylogenetic Eigenvector Mapping (PEM) was proposed, with the main advantage of explicitly incorporating a model-based warping in phylogenetic distance in which an Ornstein-Uhlenbeck (O-U) process is fitted to data before eigenvector extraction. Here we compared PVR and PEM in respect to estimated phylogenetic signal, correlated evolution under alternative evolutionary models and phylogenetic imputation, using simulated data. Despite similarity between the two approaches, PEM has a slightly higher prediction ability and is more general than the original PVR. Even so, in a conceptual sense, PEM may provide a technique in the best of both worlds, combining the flexibility of data-driven and empirical eigenfunction analyses and the sounding insights provided by evolutionary models well known in comparative analyses.     

Should I stay or should I go? Pollinator shifts rather than cospeciation dominate the evolutionary history of South African Rediviva bees and their Diascia host plants

Plant–pollinator interactions are often highly specialised, which may be a consequence of co‐evolution. Yet when plants and pollinators co‐evolve, it is not clear if this will also result in frequent cospeciation. Here, we investigate the mutual evolutionary history of South African oil‐collecting Rediviva bees and their Diascia host plants, in which the elongated forelegs of female Rediviva have been suggested to coevolve with the oil‐producing spurs of their Diascia hosts. After controlling for phylogenetic nonindependence, we found Rediviva foreleg length to be significantly correlated with Diascia spur length, suggestive of co‐evolution. However, as trait correlation could also be due to pollinator shifts, we tested if cospeciation or pollinator shifts have dominated the evolution of Rediviva–Diascia interactions by analysing phylogenies in a cophylogenetic framework. Distance‐based cophylogenetic analyses (PARAFIT, PACo) indicated significant congruence of the two phylogenies under most conditions. Yet, we found that phylogenetic relatedness was correlated with ecological similarity (the spectrum of partners that each taxon interacted with) only for Diascia but not for Rediviva, suggesting that phylogenetic congruence might be due to phylogenetic tracking by Diascia of Rediviva rather than strict (reciprocal) co‐evolution. Furthermore, event‐based reconciliation using a parsimony approach (CORE‐PA) on average revealed only 11–13 cospeciation events but 58–80 pollinator shifts. Probabilistic cophylogenetic analyses (COALA) supported this trend (8–29 cospeciations vs. 40 pollinator shifts). Our study suggests that diversification of Diascia has been largely driven by Rediviva (phylogenetic tracking, pollinator shifts) but not vice versa. Moreover, our data suggest that, even in co‐evolving mutualisms, cospeciation events might occur only infrequently.     

Phylogeny and biogeography in the evolution of migration: shorebirds of the Charadrius complex

Aim We explore whether molecular phylogeny and biogeography can complement evolutionary ecology in developing a method to address a long-standing issue in the evolution of migration: have migrations between breeding and non-breeding grounds, which may be on different continents, evolved through origins in the breeding grounds with successive shifts of the non-breeding distribution or vice versa? Methods To accommodate the biology of migration, we treated breeding and non-breeding distributions as characters to be mapped onto a phylogeny derived from mitochondrial DNA sequence data and so examined the ancestral home issue as a study in the direction of character evolution. Results Our main findings from applying this approach to a subset of the Charadrius complex of shorebirds (Aves: Charadriinae) are that a case can be made for shifts of breeding distributions having occurred in the ancestries of C. alexandrinus and C. veredus as those species evolved their present migration patterns. Our results also argue for a southern hemisphere origin (specifically South America) for the Charadrius complex as a whole. A South American origin implies other shifts in breeding distributions having occurred in the evolution of the species C. semipalmatus and C. vociferus. On applying the methods we developed for dealing with phylogenetic uncertainty, these results are reinforced and the merit of testing them further is suggested. Conclusions By way of a new approach to the evolution of migration, our study adds to a consensus emerging from the evolutionary ecology of migrant birds, arguing that shifts of breeding distributions are commonly, though not necessarily exclusively, involved in the evolution of migration.     

Assessing among‐lineage variability in phylogenetic imputation of functional trait datasets

Phylogenetic imputation has recently emerged as a potentially powerful tool for predicting missing data in functional traits datasets. As such, understanding the limitations of phylogenetic modelling in predicting trait values is critical if we are to use them in subsequent analyses. Previous studies have focused on the relationship between phylogenetic signal and clade‐level prediction accuracy, yet variability in prediction accuracy among individual tips of phylogenies remains largely unexplored. Here, we used simulations of trait evolution along the branches of phylogenetic trees to show how the accuracy of phylogenetic imputations is influenced by the combined effects of 1) the amount of phylogenetic signal in the traits and 2) the branch length of the tips to be imputed. Specifically, we conducted cross‐validation trials to estimate the variability in prediction accuracy among individual tips on the phylogenies (hereafter ‘tip‐level accuracy’). We found that under a Brownian motion model of evolution (BM, Pagel't λ = 1), tip‐level accuracy rapidly decreased with increasing tip branch‐lengths, and only tips of approximately 10% or less of the total height of the trees showed consistently accurate predictions (i.e. cross‐validation R‐squared >0.75). When phylogenetic signal was weak, the effect of tip branch‐length was reduced, becoming negligible for traits simulated with λ < 0.7, where accuracy was in any case low. Our study shows that variability in prediction accuracy among individual tips of the phylogeny should be considered when evaluating the reliability of phylogenetically imputed trait values. To address this challenge, we describe a Monte Carlo‐based method that allows one to estimate the expected tip‐level accuracy of phylogenetic predictions for continuous traits. Our approach identifies gaps in functional trait datasets for which phylogenetic imputation performs poorly, and will help ecologists to design more efficient trait collection campaigns by focusing resources on lineages whose trait values are more uncertain.     

Bias in phylogenetic measurements of extinction and a case study of end‐Permian tetrapods

Extinction risk in the modern world and extinction in the geological past are often linked to aspects of life history or other facets of biology that are phylogenetically conserved within clades. These links can result in phylogenetic clustering of extinction, a measurement comparable across different clades and time periods that can be made in the absence of detailed trait data. This phylogenetic approach is particularly suitable for vertebrate taxa, which often have fragmentary fossil records, but robust, cladistically‐inferred trees. Here we use simulations to investigate the adequacy of measures of phylogenetic clustering of extinction when applied to phylogenies of fossil taxa while assuming a Brownian motion model of trait evolution. We characterize expected biases under a variety of evolutionary and analytical scenarios. Recovery of accurate estimates of extinction clustering depends heavily on the sampling rate, and results can be highly variable across topologies. Clustering is often underestimated at low sampling rates, whereas at high sampling rates it is always overestimated. Sampling rate dictates which cladogram timescaling method will produce the most accurate results, as well as how much of a bias ancestor–descendant pairs introduce. We illustrate this approach by applying two phylogenetic metrics of extinction clustering (Fritz and Purvis's D and Moran's I) to three tetrapod clades across an interval including the Permo‐Triassic mass extinction event. These groups consistently show phylogenetic clustering of extinction, unrelated to change in other quantitative metrics such as taxonomic diversity or extinction intensity.     

PHYLOGENETIC CONSTRAINTS IN KEY FUNCTIONAL TRAITS BEHIND SPECIES’ CLIMATE NICHES: PATTERNS OF DESICCATION AND COLD RESISTANCE ACROSS 95 DROSOPHILA SPECIES

Species distributions are often constrained by climatic tolerances that are ultimately determined by evolutionary history and/or adaptive capacity, but these factors have rarely been partitioned. Here, we experimentally determined two key climatic niche traits (desiccation and cold resistance) for 92–95 Drosophila species and assessed their importance for geographic distributions, while controlling for acclimation, phylogeny, and spatial autocorrelation. Employing an array of phylogenetic analyses, we documented moderate‐to‐strong phylogenetic signal in both desiccation and cold resistance. Desiccation and cold resistance were clearly linked to species distributions because significant associations between traits and climatic variables persisted even after controlling for phylogeny. We used different methods to untangle whether phylogenetic signal reflected phylogenetically related species adapted to similar environments or alternatively phylogenetic inertia. For desiccation resistance, weak phylogenetic inertia was detected; ancestral trait reconstruction, however, revealed a deep divergence that could be traced back to the genus level. Despite drosophilids’ high evolutionary potential related to short generation times and high population sizes, cold resistance was found to have a moderate‐to‐high level of phylogenetic inertia, suggesting that evolutionary responses are likely to be slow. Together these findings suggest species distributions are governed by evolutionarily conservative climate responses, with limited scope for rapid adaptive responses to future climate change.     

Phenotypic traits evolution and morphological traits associated with echolocation calls in cryptic horseshoe bats (Rhinolophidae)

Bats provide an excellent casestudy for studying evolution due to their remarkable flight and echolocation capabilities. In this study, we sought to understand the phenotypic evolution of key traits in Rhinolophidae (horseshoe bats) using phylogenetic comparative methods. We aimed to test the phylogenetic signals of traits, and evaluated the best-fit evolutionary models given the data for each trait considering different traits may evolve under different models (i.e., Brownian Motion [BM], Ornstein-Uhlenbeck [OU], and Early Burst [EB]) and reconstruct ancestral character states. We examined how phenotypic characters are associated with echolocation calls and minimum detectable prey size. We measured 34 traits of 10 Asian rhinolophids species (187 individuals). We found that the majority of traits showed a high phylogenetic signal based on Blomberg′s K and Pagel′s λ, but each trait may evolve under different evolutionary models. Sella traits were shown to evolve under stabilizing selection based on OU models, indicating sella traits have the tendency to move forward along the branches toward some medial value in equilibrium. Our findings highlight the importance of sella characters in association with echolocation call emissions in Rhinolophidae, as calls are important for spatial cognition and also influence dietary preferences. Minimum detectable prey size in Rhinolophidae was associated with call frequency, bandwidth, call duration, wingspan, and wing surface area. Ultimately, understanding trait evolution requires sensitivity due to the differential selective pressures which may apply to different characteristics.     

The evolutionary potential of developmental instability

Whether or not developmental instability (DI) has evolutionary potential is subject to much debate. Generally, studies fail to detect significant heritability for fluctuating asymmetry (FA), a trait assumed to reflect DI. In addition, between‐trait correlations in FA are low, suggesting that DI is trait‐ rather than individual‐specific. Among the various attempts to explain these patterns, the overall weak correlation between FA and DI at the individual level has received most attention. Presently, the concept of hypothetical repeatability (R) of individual FA allows us to correct for this weak relationship, transforming patterns of FA into unbiased patterns of DI. By applying R to data presented in the literature, we show that heritability of DI remains lower than predicted but between‐trait correlations in DI substantially increase after transformation. We further provide evidence that DI changes from a trait‐ to an individual‐specific property with higher values of R. As increasing hypothetical repeatability might co‐occur with increased environmental or genetic stress, we discuss the potential implications of our results for the study of evolution of stress resistance. From this we conclude that there is an urgent need for studies that compare the evolutionary potential of developmental instability under a variety of stress conditions.     

phylosem: A fast and simple R package for phylogenetic inference and trait imputation using phylogenetic structural equation models

Phylogenetic comparative methods (PCMs) can be used to study evolutionary relationships and trade-offs among species traits. Analysts using PCM may want to (1) include latent variables, (2) estimate complex trait interdependencies, (3) predict missing trait values, (4) condition predicted traits upon phylogenetic correlations and (5) estimate relationships as slope parameters that can be compared with alternative regression methods. The Comprehensive R Archive Network (CRAN) includes well-documented software for phylogenetic linear models (phylolm), phylogenetic path analysis (phylopath), phylogenetic trait imputation (Rphylopars) and structural equation models (sem), but none of these can simultaneously accomplish all five analytical goals. We therefore introduce a new package phylosem for phylogenetic structural equation models (PSEM) and summarize features and interface. We also describe new analytical options, where users can specify any combination of Ornstein-Uhlenbeck, Pagel's-δ and Pagel's-λ transformations for species covariance. For the first time, we show that PSEM exactly reproduces estimates (and standard errors) for simplified cases that are feasible in sem, phylopath, phylolm and Rphylopars and demonstrate the approach by replicating a well-known case study involving trade-offs in plant energy budgets.     

Floral scent evolution in the section Pseudophrys: pollinator‐mediated selection or phylogenetic constraints?

• Sexually deceptive orchid species from the Mediterranean genus Ophrys usually interact with one or a few pollinator species by means of specific floral scents. In this study, we investigated the respective role of pollinator‐mediated selection and phylogenetic constraints in the evolution of floral scents in the section Pseudophrys.
• We built a phylogenetic tree of 19 Pseudophrys species based on three nuclear loci; we gathered a dataset on their pollination interactions from the literature and from our own field data; and we extracted and analysed their floral scents using solid phase microextraction and gas chromatography‐mass spectrometry. We then quantified the phylogenetic signal carried by floral scents and investigated the link between plant–pollinator interactions and floral scent composition using phylogenetic comparative methods.
• We confirmed the monophyly of the section Pseudophrys and demonstrated the existence of three main clades within this section. We found that floral scent composition is affected by both phylogenetic relationships among Ophrys species and pollination interactions, with some compounds (especially fatty acid esters) carrying a significant phylogenetic signal and some (especially alkenes and alkadienes) generating dissimilarities between closely related Pseudophrys pollinated by different insects.
• Our results show that in the section Pseudophrys, floral scents are shaped both by pollinator‐mediated selection and by phylogenetic constraints, but that the relative importance of these two evolutionary forces differ among compound classes, probably reflecting distinct selective pressures imposed upon behaviourally active and non‐active compounds.

     

Phylogenetic and ecological structure of Mediterranean caddisfly communities at various spatio‐temporal scales

Aim The evolutionary processes structuring the composition of communities remain unclear due to the complexity of factors active at various spatial and temporal scales. Here, we conducted ecological and evolutionary analyses of communities of caddisflies in the genus Hydropsyche (Insecta: Trichoptera) composed of ecomorphologically differentiated species. Location River ecosystems in the Iberian Peninsula and northern Morocco. Methods Nineteen environmental variables were assessed at 180 local study sites and species presence/absence at these sites was used to determine their ecological niche. The evolutionary framework for all 19 species of Hydropsyche encountered was generated by phylogenetic analysis of the mitochondrial cytochrome c oxidase subunit I gene and three nuclear genes: wingless, elongation factor 1‐alpha and 28S RNA. The phylogenetic tree was used: (1) to assess evolutionary niche conservatism by ecological trait correlation with the tree; and (2) to analyse the phylogenetic relatedness of community member species, at three spatial scales (local stream reaches, drainage basins, biogeographical regions). Results Ecological measurements grouped most species into either headwater, mid‐stream or lowland specialists, and traits presumably relevant to river zonation were found to be phylogenetically conservative. Species assemblages at local stream reaches were mostly mono‐ or dispecific. Species diversity increased at larger spatial scales, by adding species with non‐overlapping ecological niches at the level of river basins and by turnover of anciently differentiated lineages at the level of biogeographical regions. This indicates the effects of competition and niche filtering on community structure locally, and ancient ecological diversification and allopatric speciation, respectively, in building up the species pool at basin and biogeographical scales. Main conclusions The study demonstrates the importance of scale (grain size) in studying what determines community composition. Current ecological factors (i.e. competitive exclusion) in Hydropsyche were evident only when studying narrow local sites, while studies of assemblages at larger spatial scales instead demonstrated the roles of ecological niche differentiation, phylogenetic history of trait diversification and allopatric speciation. Increasing the grain size of investigation reveals different portions of correlated spatial and evolutionary processes.     

Phylogenetic structural equation modelling reveals no need for an ‘origin’ of the leaf economics spectrum

The leaf economics spectrum (LES) is a prominent ecophysiological paradigm that describes global variation in leaf physiology across plant ecological strategies using a handful of key traits. Nearly a decade ago, Shipley et al. (2006) used structural equation modelling to explore the causal functional relationships among LES traits that give rise to their strong global covariation. They concluded that an unmeasured trait drives LES covariation, sparking efforts to identify the latent physiological trait underlying the ‘origin’ of the LES. Here, we use newly developed phylogenetic structural equation modelling approaches to reassess these conclusions using both global LES data as well as data collected across scales in the genus Helianthus. For global LES data, accounting for phylogenetic non‐independence indicates that no additional unmeasured traits are required to explain LES covariation. Across datasets in Helianthus, trait relationships are highly variable, indicating that global‐scale models may poorly describe LES covariation at non‐global scales.     

A new phylogenetic test for comparing multiple high‐dimensional evolutionary rates suggests interplay of evolutionary rates and modularity in lanternfishes (Myctophiformes; Myctophidae)

The interplay between evolutionary rates and modularity influences the evolution of organismal body plans by both promoting and constraining the magnitude and direction of trait response to ecological conditions. However, few studies have examined whether the best‐fit hypothesis of modularity is the same as the shape subset with the greatest difference in evolutionary rate. Here, we develop a new phylogenetic comparative method for comparing evolutionary rates among high‐dimensional traits, and apply this method to analyze body shape evolution in bioluminescent lanternfishes. We frame the study of evolutionary rates and modularity through analysis of three hypotheses derived from the literature on fish development, biomechanics, and bioluminescent communication. We show that a development‐informed partitioning of shape exhibits the greatest evolutionary rate differences among modules, but that a hydrodynamically informed partitioning is the best‐fit modularity hypothesis. Furthermore, we show that bioluminescent lateral photophores evolve at a similar rate as, and are strongly integrated with, body shape in lanternfishes. These results suggest that overlapping life‐history constraints on development and movement define axes of body shape evolution in lanternfishes, and that the positions of their lateral photophore complexes are likely a passive outcome of the interaction of these ecological pressures.     

Shifts in diversification rates and host jump frequencies shaped the diversity of host range among Sclerotiniaceae fungal plant pathogens

The range of hosts that a parasite can infect in nature is a trait determined by its own evolutionary history and that of its potential hosts. However, knowledge on host range diversity and evolution at the family level is often lacking. Here, we investigate host range variation and diversification trends within the Sclerotiniaceae, a family of Ascomycete fungi. Using a phylogenetic framework, we associate diversification rates, the frequency of host jump events and host range variation during the evolution of this family. Variations in diversification rate during the evolution of the Sclerotiniaceae define three major macro‐evolutionary regimes with contrasted proportions of species infecting a broad range of hosts. Host–parasite cophylogenetic analyses pointed towards parasite radiation on distant hosts long after host speciation (host jump or duplication events) as the dominant mode of association with plants in the Sclerotiniaceae. The intermediate macro‐evolutionary regime showed a low diversification rate, high frequency of duplication events and the highest proportion of broad host range species. Our findings suggest that the emergence of broad host range fungal pathogens results largely from host jumps, as previously reported for oomycete parasites, probably combined with low speciation rates. These results have important implications for our understanding of fungal parasites evolution and are of particular relevance for the durable management of disease epidemics.     

You stay,but I Hop: Host shifting near and far co‐dominated the evolution of Enchenopa treehoppers

The importance and prevalence of phylogenetic tracking between hosts and dependent organisms caused by co‐evolution and shifting between closely related host species have been debated for decades. Most studies of phylogenetic tracking among phytophagous insects and their host plants have been limited to insects feeding on a narrow range of host species. However, narrow host ranges can confound phylogenetic tracking (phylogenetic tracking hypothesis) with host shifting between hosts of intermediate relationship (intermediate hypothesis). Here, we investigated the evolutionary history of the Enchenopa binotata complex of treehoppers. Each species in this complex has high host fidelity, but the entire complex uses hosts across eight plant orders. The phylogenies of E. binotata were reconstructed to evaluate whether (1) tracking host phylogeny; or (2) shifting between intermediately related host plants better explains the evolutionary history of E. binotata. Our results suggest that E. binotata primarily shifted between both distant and intermediate host plants regardless of host phylogeny and less frequently tracked the phylogeny of their hosts. These findings indicate that phytophagous insects with high host fidelity, such as E. binotata, are capable of adaptation not only to closely related host plants but also to novel hosts, likely with diverse phenology and defense mechanisms.