Andreas Prinzing

Ecophylogenetics: advances and perspectives

Ecophylogenetics can be viewed as an emerging fusion of ecology, biogeography and macroevolution. This new and fast‐growing field is promoting the incorporation of evolution and historical contingencies into the ecological research agenda through the widespread use of phylogenetic data. Including phylogeny into ecological thinking represents an opportunity for biologists from different fields to collaborate and has provided promising avenues of research in both theoretical and empirical ecology, towards a better understanding of the assembly of communities, the functioning of ecosystems and their responses to environmental changes. The time is ripe to assess critically the extent to which the integration of phylogeny into these different fields of ecology has delivered on its promise. Here we review how phylogenetic information has been used to identify better the key components of species interactions with their biotic and abiotic environments, to determine the relationships between diversity and ecosystem functioning and ultimately to establish good management practices to protect overall biodiversity in the face of global change. We evaluate the relevance of information provided by phylogenies to ecologists, highlighting current potential weaknesses and needs for future developments. We suggest that despite the strong progress that has been made, a consistent unified framework is still missing to link local ecological dynamics to macroevolution. This is a necessary step in order to interpret observed phylogenetic patterns in a wider ecological context. Beyond the fundamental question of how evolutionary history contributes to shape communities, ecophylogenetics will help ecology to become a better integrative and predictive science.

Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches

The question ‘what renders a species extinction prone’ is crucial to biologists. Ecological specialization has been suggested as a major constraint impeding the response of species to environmental changes. Most neoecological studies indicate that specialists suffer declines under recent environmental changes. This was confirmed by many paleoecological studies investigating longer-term survival. However, phylogeneticists, studying the entire histories of lineages, showed that specialists are not trapped in evolutionary dead ends and could even give rise to generalists. Conclusions from these approaches diverge possibly because (i) of approach-specific biases, such as lack of standardization for sampling efforts (neoecology), lack of direct observations of specialization (paleoecology), or binary coding and prevalence of specialists (phylogenetics); (ii) neoecologists focus on habitat specialization; (iii) neoecologists focus on extinction of populations, phylogeneticists on persistence of entire clades through periods of varying extinction and speciation rates; (iv) many phylogeneticists study species in which specialization may result from a lack of constraints. We recommend integrating the three approaches by studying common datasets, and accounting for range-size variation among species, and we suggest novel hypotheses on why certain specialists may not be particularly at risk and consequently why certain generalists deserve no less attention from conservationists than specialists.

Less lineages - more trait variation: phylogenetically clustered plant communities are functionally more diverse

Functional diversity within communities may influence ecosystem functioning, but which factors drive functional diversity? We hypothesize that communities assembled from many phylogenetic lineages show large functional diversity if assembly is random, but low functional diversity if assembly is controlled by interactions between species within lineages. We combined > 9000 descriptions of Dutch plant communities, a species-level phylogeny, and information on 16 functional traits (including eight dispersal traits). We found that all traits were conserved within lineages, but nevertheless communities assembled from many lineages showed a smaller variation in trait-states of most traits (including dispersal traits) than communities assembled from few lineages. Hence, within lineages, species are not randomly assembled into communities, contradicting Neutral Theory. In fact, we find evidence for evolutionary divergence in trait-states as well as present-day mutual exclusion among related, similar species, suggesting that functional diversity of communities increased due to past and present interactions between species within lineages.

Phylogenetically Poor Plant Communities Receive More Alien Species, Which More Easily Coexist with Natives

Alien species can be a major threat to ecological communities, but we do not know why some community types allow the entry of many more alien species than do others. Here, for the first time, we suggest that evolutionary diversity inherent to the constituent species of a community may determine its present receptiveness to alien species. Using recent large databases from observational studies, we find robust evidence that assemblage of plant community types from few phylogenetic lineages (in plots without aliens) corresponds to higher receptiveness to aliens. Establishment of aliens in phylogenetically poor communities corresponds to increased phylogenetic dispersion of recipient communities and to coexistence with rather than replacement of natives. This coexistence between natives and distantly related aliens in recipient communities of low phylogenetic dispersion may reflect patterns of trait assembly. In communities without aliens, low phylogenetic dispersion corresponds to increased dispersion of most traits, and establishment of aliens corresponds to increased trait concentration. We conclude that if quantified across the tree of life, high biodiversity correlates with decreasing receptiveness to aliens. Low phylogenetic biodiversity, in contrast, facilitates coexistence between natives and aliens even if they share similar trait states.

Native Fauna on Exotic Trees: Phylogenetic Conservatism and Geographic Contingency in Two Lineages of Phytophages on Two Lineages of Trees

The relative roles of evolutionary history and geographical and ecological contingency for community assembly remain unknown. Plant species, for instance, share more phytophages with closer relatives (phylogenetic conservatism), but for exotic plants introduced to another continent, this may be overlaid by geographically contingent evolution or immigration from locally abundant plant species (mass effects). We assessed within local forests to what extent exotic trees (Douglas‐fir, red oak) recruit phytophages (Coleoptera, Heteroptera) from more closely or more distantly related native plants. We found that exotics shared more phytophages with natives from the same major plant lineage (angiosperms vs. gymnosperms) than with natives from the other lineage. This was particularly true for Heteroptera, and it emphasizes the role of host specialization in phylogenetic conservatism of host use. However, for Coleoptera on Douglas‐fir, mass effects were important: immigration from beech increased with increasing beech abundance. Within a plant phylum, phylogenetic proximity of exotics and natives increased phytophage similarity, primarily in younger Coleoptera clades on angiosperms, emphasizing a role of past codiversification of hosts and phytophages. Overall, phylogenetic conservatism can shape the assembly of local phytophage communities on exotic trees. Whether it outweighs geographic contingency and mass effects depends on the interplay of phylogenetic scale, local abundance of native tree species, and the biology and evolutionary history of the phytophage taxon.

Assessing the relative importance of dispersal in plant communities using an ecoinformatics approach

Increased insight into the factors that determine the importance of dispersal limitation on species richness and species composition is of paramount importance for conservation and restoration ecology. One way to explore the importance of dispersal limitation is to use seed-sowing experiments, but these do not enable the screening of large sets of species and habitats. In the present paper we present a complementary approach based on comparing small plots with larger regions with regard to species composition and distribution of functional traits. We developed a GIS tool based on ecological and geographical criteria to quantify species pools at various spatial scales. In this GIS tool, containing floristic, large databases, phytosociological and functional information are exploited. Our premise is that differences in the nature of the species in local and regional species pools with regard to functional traits can give important clues to the processes at work in the assembly of communities.We illustrate the approach with a case study for mesotrophic hay meadows (Calthion palustris). We tested the effects of differences in frequency in the local Habitat Species Pool and differences in dispersal and persistence traits of species on local species composition. Our results show that both species pool effects and functional traits affect the probability of occurrence in small plots. Species with a high propagule weight have, given the frequency in the Local Habitat Species Pool, a lower probability of occurrence in small plots. The probability of local occurrence, however, is increased by the ability to form a persistent soil seed bank and by adult longevity. This provides support for the view that the degree of dispersal limitation is dependent on the degree of spatial isolation of the focal site relative to source populations and moreover that species inherently differ in the degree to which dispersal limitation is a limiting factor for local occurrence.

Phytophagy on phylogenetically isolated trees: why hosts should escape their relatives.

Hosts belonging to the same species suffer dramatically different impacts from their natural enemies. This has been explained by host neighbourhood, that is, by surrounding host-species diversity or spatial separation between hosts. However, even spatially neighbouring hosts may be separated by many million years of evolutionary history, potentially reducing the establishment of natural enemies and their impact. We tested whether phylogenetic isolation of oak hosts from neighbouring trees within a forest canopy reduces phytophagy. We found that an increase in phylogenetic isolation by 100 million years corresponded to a 10-fold decline in phytophagy. This was not due to poorer living conditions for phytophages on phylogenetically isolated oaks. Neither species diversity of neighbouring trees nor spatial distance to the closest oak affected phytophagy. We suggest that reduced pressure by natural enemies is a major advantage for individuals within a host species that leave their ancestral niche and grow among distantly related species.

Use of Shifting Microclimatic Mosaics by Arthropods on Exposed Tree Trunks

Abstract This study focused on two questions relevant to ecophysiology: Do distributions of animal species track shifting microclimatic mosaics under field conditions? Do distributions on different levels of spatial resolution (different “scales”) consistently modify a species’ access to heat or humidity? I counted the arthropods on the bark of exposed tree trunks in northern Germany with a 10× lens and investigated how the dominant species (collembolans, psocopterans, isopods, a linyphiid spider, and an oribatid mite) used climatic patterns at various scales. These included mesoclimatic patterns and shifting microclimatic patterns such as microrelief, trunk faces, and trunk/mesoclimate differences. Bias owing to changing frequency of microhabitats, or to redistributions of animals between microhabitats was avoided. I also investigated the effects of climatic patterns on heat and humidity levels at the bark surface. The distributions of all species, except the psocopterans, similarly tracked shifting microclimatic mosaics and mesoclimates. The distributions of most species modified their access to heat or humidity consistently at several mutually independent scales. The remaining species seemed to be restricted in their climate use by sensory or metabolic limitations.

Woody plants in Kenya: expanding the Higher-Taxon Approach

Abstract Information on species diversity is urgently needed but often unavailable. Conservation biologists have therefore used the ‘Higher-Taxon Approach’ to predict the distribution of α-diversity of species from the diversities of higher taxa. We expanded this approach. We studied the Kenyan woody plant flora on a 56×56 km grid basis and found that the distribution of species α-diversity could be predicted precisely even from ordinal diversity. In contrast, the distribution of species β-diversity was difficult to predict even from the genus level, although within biogeographic zones the prediction improved. The spatial scale of species α-diversity could be predicted precisely only from genus level, and was hardly predictable from ordinal level. The spatial scale of species β-diversity was roughly predictable from genus to ordinal levels. Overall, the Higher-Taxon Approach could be expanded to a rough prediction of the spatial scale of species diversities. But, the approach only poorly predicted the spatial distribution of species β-diversity.

The relationship between global and regional distribution diminishes among phylogenetically basal species

Abstract Phylogenetic legacy and phylogenetic trends affect the ecology of species‐except, apparently, for the width of their distribution. As a result, “macroecological”patterns of species distributions emerge constantly in phylogenetically very distinct species assemblages. The width of the global distribution of species, for instance, constantly correlates positively to the width of their regional distribution. However, such patterns primarily reflect the phylogenetically derived species that dominate most assemblages. Basal species, in contrast, might show different macroecological patterns. We tested the hypothesis that the correlation between global and regional distributions of species diminishes among the phylogenetically basal species. We considered central European higher plants and defined global distribution as the occupancy of global floristic zones, regional distribution as the grid occupancy in Eastern Germany, and phylogenetic position as the rank distance to tree base. We also took into account a number of confounding variables. We found that, across all lineages, the global/regional correlation diminished among basal species. We then reanalyzed 19 lineages separately and always found the same pattern. The pattern reflected both increases in global distributions and decreases in regional distributions among basal species. The results indicate that many basal species face a risk of global or at least regional extinction, but have escaped the downward spiral of mutually reinforcing extinction risks at multiple scales. We suggest that many basal species had much time to expand their global ranges but are presently displaced locally by more derived species. Overall, the study shows that macroecological patterns may not be static and universal, but may undergo macroevolutionary trends. Analyses of macroecological patterns across a phylogeny may thus provide insights into macroevolutionary processes.