Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species

Ecologists are increasingly adopting an evolutionary perspective, and in recent years, the idea that closely related species are ecologically similar has become widespread. In this regard, phylogenetic signal must be distinguished from phylogenetic niche conservatism. Phylogenetic niche conservatism results when closely related species are more ecologically similar that would be expected based on their phylogenetic relationships; its occurrence suggests that some process is constraining divergence among closely related species. In contrast, phylogenetic signal refers to the situation in which ecological similarity between species is related to phylogenetic relatedness; this is the expected outcome of Brownian motion divergence and thus is necessary, but not sufficient, evidence for the existence of phylogenetic niche conservatism. Although many workers consider phylogenetic niche conservatism to be common, a review of case studies indicates that ecological and phylogenetic similarities often are not related. Consequently, ecologists should not assume that phylogenetic niche conservatism exists, but rather should empirically examine the extent to which it occurs.     

Phylogenetic signal in tooth wear dietary niche proxies

In the absence of independent observational data, ecologists and paleoecologists use proxies for the Eltonian niches of species (i.e., the resource or dietary axes of the niche). Some dietary proxies exploit the fact that mammalian teeth experience wear during mastication, due to both tooth‐on‐tooth and food‐on‐tooth interactions. The distribution and types of wear detectible at micro‐ and macroscales are highly correlated with the resource preferences of individuals and, in turn, species. Because methods that quantify the distribution of tooth wear (i.e., analytical tooth wear methods) do so by direct observation of facets and marks on the teeth of individual animals, dietary inferences derived from them are thought to be independent of the clade to which individuals belong. However, an assumption of clade or phylogenetic independence when making species‐level dietary inferences may be misleading if phylogenetic niche conservatism is widespread among mammals. Herein, we test for phylogenetic signal in data from numerous analytical tooth wear studies, incorporating macrowear (i.e., mesowear) and microwear (i.e., low‐magnification microwear and dental microwear texture analysis). Using two measures of phylogenetic signal, heritability (H²) and Pagel's λ, we find that analytical tooth wear data are not independent of phylogeny and failing to account for such nonindependence leads to overestimation of discriminability among species with different dietary preferences. We suggest that morphological traits inherited from ancestral clades (e.g., tooth shape) influence the ways in which the teeth wear during mastication and constrain the foods individuals of a species can effectively exploit. We do not suggest that tooth wear is simply phylogeny in disguise; the tooth wear of individuals and species likely varies within some range that is set by morphological constraints. We therefore recommend the use of phylogenetic comparative methods in studies of mammalian tooth wear, whenever possible.     

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.     

Phylogenetic diversity and the functioning of ecosystems

Phylogenetic diversity (PD) describes the total amount of phylogenetic distance among species in a community. Although there has been substantial research on the factors that determine community PD, exploration of the consequences of PD for ecosystem functioning is just beginning. We argue that PD may be useful in predicting ecosystem functions in a range of communities, from single-trophic to complex networks. Many traits show a phylogenetic signal, suggesting that PD can estimate the functional trait space of a community, and thus ecosystem functioning. Phylogeny also determines interactions among species, and so could help predict how extinctions cascade through ecological networks and thus impact ecosystem functions. Although the initial evidence available suggests patterns consistent with these predictions, we caution that the utility of PD depends critically on the strength of phylogenetic signals to both traits and interactions. We advocate for a synthetic approach that incorporates a deeper understanding of how traits and interactions are shaped by evolution, and outline key areas for future research. If these complexities can be incorporated into future studies, relationships between PD and ecosystem function bear promise in conceptually unifying evolutionary biology with ecosystem ecology.     

Neutral lipid fatty acid composition as trait and constraint in Collembola evolution

Functional traits determine the occurrence of species along environmental gradients and their coexistence with other species. Understanding how traits evolved among coexisting species helps to infer community assembly processes. We propose fatty acid composition in consumer tissue as a functional trait related to both food resources and physiological functions of species. We measured phylogenetic signal in fatty acid profiles of 13 field‐sampled Collembola (springtail) species and then combined the data with published fatty acid profiles of another 24 species. Collembola fatty acid profiles generally showed phylogenetic signal, with related species resembling each other. Long‐chain polyunsaturated fatty acids, related to physiological functions, demonstrated phylogenetic signal. In contrast, most food resource biomarker fatty acids and the ratios between bacterial, fungal, and plant biomarker fatty acids exhibited no phylogenetic signal. Presumably, fatty acids related to physiological functions have been constrained during Collembola evolutionary history: Species with close phylogenetic affinity experienced similar environments during divergence, while niche partitioning in food resources among closely related species favored species coexistence. Measuring phylogenetic signal in ecologically relevant traits of coexisting species provides an evolutionary perspective to contemporary assembly processes of ecological communities. Integrating phylogenetic comparative methods with community phylogenetic and trait‐based approaches may compensate for the limitations of each method when used alone and improve understanding of processes driving and maintaining assembly patterns.     

Assessing the relationships between phylogenetic and functional singularities in sharks (Chondrichthyes)

The relationships between diversity and ecosystem functioning have become a major focus of science. A crucial issue is to estimate functional diversity, as it is intended to impact ecosystem dynamics and stability. However, depending on the ecosystem, it may be challenging or even impossible to directly measure ecological functions and thus functional diversity. Phylogenetic diversity was recently under consideration as a proxy for functional diversity. Phylogenetic diversity is indeed supposed to match functional diversity if functions are conservative traits along evolution. However, in case of adaptive radiation and/or evolutive convergence, a mismatch may appear between species phylogenetic and functional singularities. Using highly threatened taxa, sharks, this study aimed to explore the relationships between phylogenetic and functional diversities and singularities. Different statistical computations were used in order to test both methodological issue (phylogenetic reconstruction) and overall a theoretical questioning: the predictive power of phylogeny for function diversity. Despite these several methodological approaches, a mismatch between phylogeny and function was highlighted. This mismatch revealed that (i) functions are apparently nonconservative in shark species, and (ii) phylogenetic singularity is not a proxy for functional singularity. Functions appeared to be not conservative along the evolution of sharks, raising the conservational challenge to identify and protect both phylogenetic and functional singular species. Facing the current rate of species loss, it is indeed of major importance to target phylogenetically singular species to protect genetic diversity and also functionally singular species in order to maintain particular functions within ecosystem.     

Evolutionary heritage shapes tree distributions along an Amazon‐to‐Andes elevation gradient

Understanding how evolutionary constraints shape the elevational distributions of tree lineages provides valuable insight into the future of tropical montane forests under global change. With narrow elevational ranges, high taxonomic turnover, frequent habitat specialization, and exceptional levels of endemism, tropical montane forests and trees are predicted to be highly sensitive to environmental change. Using plot census data from a gradient traversing > 3,000 m in elevation on the Amazonian flank of the Peruvian Andes, we employ phylogenetic approaches to assess the influence of evolutionary heritage on distribution trends of trees at the genus‐level. We find that closely related lineages tend to occur at similar mean elevations, with sister genera pairs occurring a mean 254 m in elevation closer to each other than the mean elevational difference between non‐sister genera pairs. We also demonstrate phylogenetic clustering both above and below 1,750 m a.s.l, corresponding roughly to the cloud‐base ecotone. Belying these general trends, some lineages occur across many different elevations. However, these highly plastic lineages are not phylogenetically clustered. Overall, our findings suggest that tropical montane forests are home to unique tree lineage diversity, constrained by their evolutionary heritage and vulnerable to substantial losses under environmental changes, such as rising temperatures or an upward shift of the cloud‐base.     

Larger phylogenetic distances in litter mixtures: lower microbial biomass and higher C/N ratios but equal mass loss

Phylogenetic distances of coexisting species differ greatly within plant communities, but their consequences for decomposers and decomposition remain unknown. We hypothesized that large phylogenetic distance of leaf litter mixtures increases differences of their litter traits, which may, in turn, result in increased resource complementarity or decreased resource concentration for decomposers and hence increased or decreased chemical transformation and reduction of litter. We conducted a litter mixture experiment including 12 common temperate tree species (evolutionarily separated by up to 106 Myr), and sampled after seven months, at which average mass loss was more than 50%. We found no effect of increased phylogenetic distance on litter mass loss or on abundance and diversity of invertebrate decomposers. However, phylogenetic distance decreased microbial biomass and increased carbon/nitrogen (C/N) ratios of litter mixtures. Consistently, four litter traits showed (marginally) significant phylogenetic signal and in three of these traits increasing trait difference decreased microbial biomass and increased C/N. We suggest that phylogenetic proximity of litter favours microbial decomposers and chemical transformation of litter owing to a resource concentration effect. This leads to a new hypothesis: closely related plant species occurring in the same niche should promote and profit from increased nutrient availability.     

Are phylogenies derived from family‐level supertrees robust for studies on macroecological patterns along environmental gradients?

Ecologists frequently use a supertree method to generate phylogenies in ecological studies. However, the robustness of research results based on phylogenies generated with a supertree method has not been well evaluated. Here, we use the angiosperm tree flora of North America as a model system to test the robustness of phylogenies generated with a supertree method for studies on the relationship between phylogenetic properties and environment, by comparing the relationship between phylogenetic metrics and environmental variables derived from a phylogeny reconstructed with a supertree method to that derived from a phylogeny resolved at species level. North America was divided into equal area quadrats of 12 100 km². Nine indices of phylogenetic structure were calculated for angiosperm tree assemblages in each quadrat using two phylogenies resolved at different levels (one resolved at the family level and the other resolved at the species level). Scores of phylogenetic indices were related to two major climatic variables (temperature and precipitation) using correlation and regression analyses. Scores of phylogenetic indices resulting from the two phylogenies are perfectly or nearly perfectly correlated. On average, there is no difference in the variation explained by the two climatic variables between scores of phylogenetic indices derived from the two phylogenies. Our study suggests that a phylogeny derived from a well resolved family-level supertree as backbone with genera and species attached to the backbone as polytomies is robust for studies investigating the relationship between phylogenetic structure and environment in biological assemblages at a broad spatial scale.     

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.     

Habitat filtering influences the phylogenetic structure of avian communities across a coastal gradient in southern Brazil

The evolution of a particular trait or combination of traits within lineages may affect subsequent evolutionary outcomes, leading closely related species to exhibit higher phenotypic similarity than expected under a simple Brownian‐motion evolutionary model. Niche theory postulates that phenotypes determine species distribution across environmental gradients, leading to a phylogenetic signature in the community assembly. Thus, the incorporation of species phylogeny in the analysis of community ecology structure allows one to link broader environmental, spatial and temporal factors to local, small‐scale ecological processes, thus enabling understanding of community assembly patterns in a broader context. We used the net relatedness index to assess phylogenetic structure within avian communities across a harshness gradient in coastal habitats in southern Brazil. We also evaluated phylogenetic beta diversity, to test whether closely related species exploit habitats with similar environmental conditions. In order to do so, we scaled up phylogenetic information from the species to site level using phylogenetic fuzzy weighting. We found a pattern of phylogenetic clustering in less‐vegetated habitats, namely sandy beach and dunes, which are subject to harsher conditions because of proximity to the ocean. Basal lineages were associated with the more structurally homogeneous sandy beach, while late‐divergence clades occurred in more complex habitats, which were positively related to vegetation cover and height. The observed pattern of phylogenetic clustering suggested the importance of harsh conditions in constraining the distribution of avian lineages. Furthermore, contrasting environmental features between habitats influenced phylogenetic variation, demonstrating the prevalence of phylogenetic habitat filtering. From an applied point of view, such as planning and management of biological reserves, we showed that the full array of habitat patches embedded within coastal ecological gradients must be included in order to preserve distinct evolutionary lineages.     

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.     

Parallel evolution of larval morphology and habitat in the snail-killing fly genus Tetanocera

In this study, we sequenced one nuclear and three mitochondrial DNA loci to construct a robust estimate of phylogeny for all available species of Tetanocera. Character optimizations suggested that aquatic habitat was the ancestral condition for Tetanocera larvae, and that there were at least three parallel transitions to terrestrial habitat, with one reversal. Maximum likelihood analyses of character state transformations showed significant correlations between habitat transitions and changes in four larval morphological characteristics (cuticular pigmentation and three characters associated with the posterior spiracular disc). We provide evidence that phylogenetic niche conservatism has been responsible for the maintenance of aquatic-associated larval morphological character states, and that concerted convergence and/or gene linkage was responsible for parallel morphological changes that were derived in conjunction with habitat transitions. These habitat-morphology associations were consistent with the action of natural selection in facilitating the morphological changes that occurred during parallel aquatic to terrestrial habitat transitions in Tetanocera.     

Climatic niche evolution in turtles is characterized by phylogenetic conservatism for both aquatic and terrestrial species

Understanding how the climatic niche of species evolved has been a topic of high interest in current theoretical and applied macroecological studies. However, little is known regarding how species traits might influence climatic niche evolution. Here, we evaluated patterns of climatic niche evolution in turtles (tortoises and freshwater turtles) and whether species habitat (terrestrial or aquatic) influences these patterns. We used phylogenetic, climatic and distribution data for 261 species to estimate their climatic niches. Then, we compared whether niche overlap between sister species was higher than between random species pairs and evaluated whether niche optima and rates varied between aquatic and terrestrial species. Sister species had higher values of niche overlap than random species pairs, suggesting phylogenetic climatic niche conservatism in turtles. The climatic niche evolution of the group followed an Ornstein–Uhlenbeck model with different optimum values for aquatic and terrestrial species, but we did not find consistent evidence of differences in their rates of climatic niche evolution. We conclude that phylogenetic climatic niche conservatism occurs among turtle species. Furthermore, terrestrial and aquatic species occupy different climatic niches but these seem to have evolved at similar evolutionary rates, reinforcing the importance of habitat in understanding species climatic niches and their evolution.     

Morphological and niche divergence of pinyon pines

The environmental variables that define a species ecological niche should be associated with the evolutionary patterns present in the adaptations that resulted from living in these conditions. Thus, when comparing across species, we can expect to find an association between phylogenetically independent phenotypic characters and ecological niche evolution. Few studies have evaluated how organismal phenotypes might mirror patterns of niche evolution if these phenotypes reflect adaptations. Doing so could contribute on the understanding of the origin and maintenance of phenotypic diversity observed in nature. Here, we show the pattern of niche evolution of the pinyon pine lineage (Pinus subsection Cembroides); then, we suggest morphological adaptations possibly related to niche divergence, and finally, we test for correlation between ecological niche and morphology. We demonstrate that niche divergence is the general pattern within the clade and that it is positively correlated with adaptation.