Evolutionary limits ameliorate the negative impact of an invasive plant

Invasive species can quickly transform biological communities due to their high abundance and strong impacts on native species, in part because they can be released from the ecological forces that limit native populations. However, little is known about the long-term dynamics of invasions; do invaders maintain their dominant status over long time spans, or do new ecological and evolutionary forces eventually develop to limit their populations? Alliaria petiolata is a Eurasian species that aggressively invades North American forest understories, in part due to the production of toxic phytochemicals. Here we document a marked decline in its phytotoxin production and a consequent decline in their impact on three native species, across a 50+ year chronosequence of Alliaria petiolata invasion. Genetic evidence suggests that these patterns result from natural selection for decreased phytotoxin production rather than founder effects during introduction and spread. These patterns are consistent with the finding of slowing A. petiolata population growth and rebounding native species abundance across a separate chronosequence in Illinois, U.S. These results suggest that this invader is developing evolutionary limits in its introduced range and highlight the importance of understanding the long-term processes that shape species invasions and their impacts.     

Intercontinental differences in resource use reveal the importance of mutualisms in fire ant invasions

Mutualisms play key roles in the functioning of ecosystems. However, reciprocally beneficial interactions that involve introduced species also can enhance invasion success and in doing so compromise ecosystem integrity. For example, the growth and competitive ability of introduced plant species can increase when fungal or microbial associates provide limiting nutrients. Mutualisms also may aid animal invasions, but how such systems may promote invasion success has received relatively little attention. Here we examine how access to food-for-protection mutualisms involving the red imported fire ant (Solenopsis invicta) aids the success of this prominent invader. Intense interspecific competition in its native Argentina constrained the ability of S. invicta to benefit from honeydew-producing Hemiptera (and other accessible sources of carbohydrates), whereas S. invicta dominated these resources in its introduced range in the United States. Consistent with this strong pattern, nitrogen isotopic data revealed that fire ants from populations in the United States occupy a lower trophic position than fire ants from Argentina. Laboratory and field experiments demonstrated that honeydew elevated colony growth, a crucial determinant of competitive performance, even when insect prey were not limiting. Carbohydrates, obtained largely through mutualistic partnerships with other organisms, thus represent critical resources that may aid the success of this widespread invasive species. These results illustrate the potential for mutualistic interactions to play a fundamental role in the establishment and spread of animal invasions.     

INAUGURAL ARTICLE by a Recently Elected Academy Member:Evolutionary diversification,coevolution between populations and their antagonists,and the filling of niche space

The population component of a species’ niche corresponds to the distribution of individuals across environments within a region. As evolutionary clades of species diversify, they presumably fill niche space, and, consequently, the rate of increase in species numbers slows. Total niche space and species numbers appear to be relatively stable over long periods, and so an increase in the species richness of one clade must be balanced by decrease in others. However, in several analyses, the total population niche space occupied per clade is independent of the number of species, suggesting that species in more diverse clades overlap more in niche space. This overlap appears to be accommodated by variation in the populations of each species, including their absence, within suitable niche space. I suggest that the uneven filling of niche space results from localized outcomes of the dynamic coevolutionary interactions of populations with their pathogens or other antagonists. Furthermore, I speculate that relationships with pathogens might constrain diversification if pathogen diversity increased with host diversity and resulted in more frequent host switching and emergent disease. Many indirect observations are consistent with these scenarios. However, the postulated influence of pathogens on the filling of niche space and diversification of clades primarily highlights our lack of knowledge concerning the space and time dimensions of coevolutionary interactions and their influence on population distribution and species diversification.     

Plant invasions and extinction debts

Whether introduced species invasions pose a major threat to biodiversity is hotly debated. Much of this debate is fueled by recent findings that competition from introduced organisms has driven remarkably few plant species to extinction. Instead, native plant species in invaded ecosystems are often found in refugia: patchy, marginal habitats unsuitable to their nonnative competitors. However, whether the colonization and extinction dynamics of these refugia allow long-term native persistence is uncertain. Of particular concern is the possibility that invasive plants may induce an extinction debt in the native flora, where persistence over the short term masks deterministic extinction trajectories. We examined how invader impacts on landscape structure influence native plant persistence by combining recently developed quantitative techniques for evaluating metapopulation persistence with field measurements of an invaded plant community. We found that European grass invasion of an edaphically heterogeneous California landscape has greatly decreased the likelihood of the persistence of native metapopulations. It does so via two main pathways: (i) decreasing the size of native refugia, which reduces seed production and increases local extinction, and (ii) eroding the dispersal permeability of the matrix between refugia, which reduces their connectivity. Even when native plant extinction is the deterministic outcome of invasion, the time to extinction can be on the order of hundreds of years. We conclude that the relatively short time since invasion in many parts of the world is insufficient to observe the full impact of plant invasions on native biodiversity.     

Evolution of host range in Coleosporium ipomoeae,a plant pathogen with multiple hosts

Plants and their pathogens coevolve locally. Previous investigations of one host–one pathogen systems have demonstrated that natural selection favors pathogen genotypes that are virulent on a broad range of host genotypes. In the present study, we examine a system consisting of one pathogen species that infects three host species in the morning glory genus Ipomoea. We show that many pathogen genotypes can infect two or three of the host species when tested on plants from nonlocal communities. By contrast, pathogen genotypes are highly host-specific, infecting only one host species, when tested on host species from the local community. This pattern indicates that within-community evolution narrows the host breadth of pathogen genotypes. Possible evolutionary mechanisms include direct selection for narrow host breadth due to costs of virulence and evolution of ipomoea resistance in the host species.Much of plant-pathogen coevolution is mediated by “gene-for-gene” (GFG) interactions. These interactions involve R genes in plants and corresponding virulence/avirulence genes in the pathogen (1). At a given pair of corresponding loci, a host may carry either a resistant (Res) or a susceptible (Sus) allele, or both, with Res typically being dominant. The pathogen may carry either a virulent (Vir) allele or an avirulent (Avr) allele. Infection results, unless at one pair of corresponding loci, the plant R locus has a Res allele and the pathogen has the Avr allele. Models of the evolution of GFG systems generally predict that generalist pathogens (those able to infect multiple host-resistance genotypes) will be favored by natural selection over highly specialized genotypes that can infect only one resistance genotype (2–6). Experimental analyses of pathogen host breadth in natural plant–pathogen systems are consistent with these expectations in that pathogen isolates are generally able to infect multiple host-resistance genotypes, especially in host populations with high levels of resistance (7–10).With very few exceptions (11, 12), the evolution of pathogen host range has been examined, both theoretically and empirically, for a single pathogen species interacting with a single host species. Many pathogens, however, are capable of infecting multiple host species. Predictions of evolutionary models based on a single evolving host species cannot be clearly extrapolated to this situation. Moreover, there are reasons to believe that, with multiple host species, selection for generalism may not be as prevalent. Maintaining infectivity on multiple hosts requires continued success in the coevolutionary arms race with more than one independently evolving host genome. The conditions under which this maintained infectivity can occur are likely more restrictive than with only one host, although this possibility has not been examined theoretically. In addition, selection to maintain infectivity on a particular host is likely weaker when the pathogen population can successfully reproduce on another host (see ref. 13 for an analogous argument with respect to partial resistance). Finally, costs associated with the ability to infect multiple host species (e.g., ref. 14) are likely greater than costs associated with the ability to infect multiple genotypes within the same host. All of these factors would tend to weaken selection for a broad host range and thus promote the evolution of specialist pathogen genotypes within populations.One approach to determining whether there is an evolutionary tendency for host breadth to be narrowed within populations is to compare pathogen host breadth in its local native community with host breadth on hosts from outside its native community (e.g., refs. 9 and 13). The latter constitutes an estimate of host breadth on host species with which the pathogen has presumably not recently coevolved and is also an estimate of host breadth for a pathogen strain that has recently immigrated into a new community. If evolutionary processes within local communities act to promote specialization, host breadth should be lower on hosts from the native community. In this report, we demonstrate that this pattern is exhibited for a host–pathogen system consisting of one pathogen and three host species.     

Phylogenetic escalation and decline of plant defense strategies

As the basal resource in most food webs, plants have evolved myriad strategies to battle consumption by herbivores. Over the past 50 years, plant defense theories have been formulated to explain the remarkable variation in abundance, distribution, and diversity of secondary chemistry and other defensive traits. For example, classic theories of enemy-driven evolutionary dynamics have hypothesized that defensive traits escalate through the diversification process. Despite the fact that macroevolutionary patterns are an explicit part of defense theories, phylogenetic analyses have not been previously attempted to disentangle specific predictions concerning (i) investment in resistance traits, (ii) recovery after damage, and (iii) plant growth rate. We constructed a molecular phylogeny of 38 species of milkweed and tested four major predictions of defense theory using maximum-likelihood methods. We did not find support for the growth-rate hypothesis. Our key finding was a pattern of phyletic decline in the three most potent resistance traits (cardenolides, latex, and trichomes) and an escalation of regrowth ability. Our neontological approach complements more common paleontological approaches to discover directional trends in the evolution of life and points to the importance of natural enemies in the macroevolution of species. The finding of macroevolutionary escalating regowth ability and declining resistance provides a window into the ongoing coevolutionary dynamics between plants and herbivores and suggests a revision of classic plant defense theory. Where plants are primarily consumed by specialist herbivores, regrowth (or tolerance) may be favored over resistance traits during the diversification process.     

Applying a regional community concept to forest birds of eastern North America

The regional community concept embraces the idea that species interactions across large areas shape both the geographic/ecological distributions and the local abundances of populations. Within this framework, I analyzed the distribution and abundance of 79 species of land birds across 142 ca. 10-ha census plots from standardized breeding bird censuses in deciduous and mixed forests of eastern North America. To characterize the regional ecological space, plots were ordinated on the basis of species abundances. Within the regional community defined by these synthetic axes, the distribution and abundance of individual species did not appear to be shaped by competition or to reflect the adaptations of individuals: (i) local abundance and population extent across the ordination axes were unrelated, (ii) pairwise correlation coefficients of species abundances were centered on 0, (iii) average species distribution and abundance were independent of the number of close relatives, and (iv) distribution and abundance exhibited no evolutionary (phylogenetic) conservatism. To explain these seemingly random patterns, I speculate that species are approximately evenly matched competitors over much of the region and that their distributions and relative abundances are determined by the labile coevolutionary outcomes of interactions with specialized pathogens. Thus, despite the appearance that random processes determine patterns in the distribution and abundance of populations in the regional community, it is plausible that species-specific deterministic interactions are responsible. Although competition is a dominant force in ecological communities, variation in the distribution and abundance of individual species might instead reflect the outcome of interactions with specialized antagonists, including pathogens.     

Resolving postglacial phylogeography using high-throughput sequencing

The distinction between model and nonmodel organisms is becoming increasingly blurred. High-throughput, second-generation sequencing approaches are being applied to organisms based on their interesting ecological, physiological, developmental, or evolutionary properties and not on the depth of genetic information available for them. Here, we illustrate this point using a low-cost, efficient technique to determine the fine-scale phylogenetic relationships among recently diverged populations in a species. This application of restriction site-associated DNA tags (RAD tags) reveals previously unresolved genetic structure and direction of evolution in the pitcher plant mosquito, Wyeomyia smithii, from a southern Appalachian Mountain refugium following recession of the Laurentide Ice Sheet at 22,000–19,000 B.P. The RAD tag method can be used to identify detailed patterns of phylogeography in any organism regardless of existing genomic data, and, more broadly, to identify incipient speciation and genome-wide variation in natural populations in general.     

More closely related species are more ecologically similar in an experimental test

The relationship between phylogenetic distance and ecological similarity is key to understanding mechanisms of community assembly, a central goal of ecology. The field of community phylogenetics uses phylogenetic information to infer mechanisms of community assembly; we explore, the underlying relationship between phylogenetic similarity and the niche. We combined a field experiment using 32 native plant species with a molecular phylogeny and found that closely related plant species shared similar germination and early survival niches. Species also competed more with close relatives than with distant relatives in field soils; however, in potting soil this pattern reversed, and close relatives might even have more mutalistic relationships than distant relatives in these soils. Our results suggest that niche conservatism (habitat filtering) and species interactions (competition or facilitation) structure community composition, that phylogenetic relationships influence the strength of species' interactions, and that conserved aspects of plant niches include soil attributes.     

From the Cover: Plant and Insect Biodiversity Special Feature: Phylogenetic and trait similarity to a native species predict herbivory on non-native oaks

Introduced plants tend to experience less herbivory than natives, although herbivore loads vary widely. Herbivores may switch hosts onto an introduced plant for at least two reasons. They may recognize the novel plant as a potential host based on similarity of the plant''s traits to the traits of one of its native hosts, a similarity that may or may not exhibit phylogenetic signal. Alternatively, herbivores may feed optimally, assessing which introduced plants provide the best nutrition irrespective of similarity to native species. Here, we created a phylogeny of 57 oak (Quercus) taxa, which were grown outside of their ranges in a common botanical garden that contained one abundant native oak (Quercus lobata). We used the phylogeny to estimate the phylogenetic conservatism of herbivory by two feeding guilds of insects (leaf chewers and leaf miners) and 11 plant traits expected to affect herbivore performance. We found high phylogenetic signal in chewing damage but not mining damage and all traits except for leaf maturation time. Introduced oaks that are more closely related to the native oak received more chewing and mining damage than distantly related oaks, and introduced oaks that had greater overall similarity in leaf traits also received higher chewing damage but not mining damage. These results demonstrate that interactions between introduced plants and their herbivores are driven independently by traits that track plant phylogeny and leaf traits that likely affect herbivore performance.     

Macroevolution and the biological diversity of plants and herbivores

Terrestrial biodiversity is dominated by plants and the herbivores that consume them, and they are one of the major conduits of energy flow up to higher trophic levels. Here, we address the processes that have generated the spectacular diversity of flowering plants (>300,000 species) and insect herbivores (likely >1 million species). Long-standing macroevolutionary hypotheses have postulated that reciprocal evolution of adaptations and subsequent bursts of speciation have given rise to much of this biodiversity. We critically evaluate various predictions based on this coevolutionary theory. Phylogenetic reconstruction of ancestral states has revealed evidence for escalation in the potency or variety of plant lineages'' chemical defenses; however, escalation of defense has been moderated by tradeoffs and alternative strategies (e.g., tolerance or defense by biotic agents). There is still surprisingly scant evidence that novel defense traits reduce herbivory and that such evolutionary novelty spurs diversification. Consistent with the coevolutionary hypothesis, there is some evidence that diversification of herbivores has lagged behind, but has nevertheless been temporally correlated with that of their host-plant clades, indicating colonization and radiation of insects on diversifying plants. However, there is still limited support for the role of host-plant shifts in insect diversification. Finally, a frontier area of research, and a general conclusion of our review, is that community ecology and the long-term evolutionary history of plant and insect diversification are inexorably intertwined.     

Exotic taxa less related to native species are more invasive

Some species introduced into new geographical areas from their native ranges wreak ecological and economic havoc in their new environment. Although many studies have searched for either species or habitat characteristics that predict invasiveness of exotic species, the match between characteristics of the invader and those of members of the existing native community may be essential to understanding invasiveness. Here, we find that one metric, the phylogenetic relatedness of an invader to the native community, provides a predictive tool for invasiveness. Using a phylogenetic supertree of all grass species in California, we show that highly invasive grass species are, on average, significantly less related to native grasses than are introduced but noninvasive grasses. The match between the invader and the existing native community may explain why exotic pest species are not uniformly noxious in all novel habitats. Relatedness of invaders to the native biota may be one useful criterion for prioritizing management efforts of exotic species.     

Specificity and transmission mosaic of ant nest-wall fungi

Mutualism, whereby species interact to their mutual benefit, is extraordinary in a competitive world. To recognize general patterns of origin and maintenance from the plethora of mutualistic associations proves a persisting challenge. The simplest situation is believed to be that of a single mutualist specific to a single host, vertically transmitted from one host generation to the next. We characterized ascomycete fungal associates cultured for nest architecture by the ant subgenera Dendrolasius and Chthonolasius. The ants probably manage their fungal mutualists by protecting them against fungal competitors. The ant subgenera display different ant-to-fungus specificity patterns, one-to-two and many-to-one, and we infer vertical transmission, in the latter case overlaid by horizontal transmission. Possible evolutionary trajectories include a reversal from fungiculture by other Lasius subgenera and inheritance of fungi through life cycle interactions of the ant subgenera. The mosaic indicates how specificity patterns can be shaped by an interplay between host life-cycles and transmission adaptations.     

Host population persistence in the face of introduced vector-borne diseases: Hawaii amakihi and avian malaria

The past quarter century has seen an unprecedented increase in the number of new and emerging infectious diseases throughout the world, with serious implications for human and wildlife populations. We examined host persistence in the face of introduced vector-borne diseases in Hawaii, where introduced avian malaria and introduced vectors have had a negative impact on most populations of Hawaiian forest birds for nearly a century. We studied birds, parasites, and vectors in nine study areas from 0 to 1,800 m on Mauna Loa Volcano, Hawaii from January to October, 2002. Contrary to predictions of prior work, we found that Hawaii amakihi (Hemignathus virens), a native species susceptible to malaria, comprised from 24.5% to 51.9% of the avian community at three low-elevation forests (55-270 m). Amakihi were more abundant at low elevations than at disease-free high elevations, and were resident and breeding there. Infection rates were 24-40% by microscopy and 55-83% by serology, with most infected individuals experiencing low-intensity, chronic infections. Mosquito trapping and diagnostics provided strong evidence for year-round local transmission. Moreover, we present evidence that Hawaii amakihi have increased in low elevation habitats on southeastern Hawaii Island over the past decade. The recent emergent phenomenon of recovering amakihi populations at low elevations, despite extremely high prevalence of avian malaria, suggests that ecological or evolutionary processes acting on hosts or parasites have allowed this species to recolonize low-elevation habitats. A better understanding of the mechanisms allowing coexistence of hosts and parasites may ultimately lead to tools for mitigating disease impacts on wildlife and human populations.     

Synergy between pathogen release and resource availability in plant invasion

Why do some exotic plant species become invasive? Two common hypotheses, increased resource availability and enemy release, may more effectively explain invasion if they favor the same species, and therefore act in concert. This would be expected if plant species adapted to high levels of available resources in their native range are particularly susceptible to enemies, and therefore benefit most from a paucity of enemies in their new range. We tested this possibility by examining how resource adaptations influence pathogen richness and release among 243 European plant species naturalized in the United States. Plant species adapted to higher resource availability hosted more pathogen species in their native range. Plants from mesic environments hosted more fungi than plants from xeric environments, and plants from nitrogen-rich environments hosted more viruses than plants from nitrogen-poor environments. Furthermore, plants classified as competitors hosted more than 4 times as many fungi and viruses as did stress tolerators. Patterns of enemy release mirrored those of pathogen richness: competitors and species from mesic and nitrogen-rich environments were released from many pathogen species, while stress tolerators and species from xeric and nitrogen-poor environments were released from relatively few pathogen species. These results suggest that enemy release contributes most to invasion by fast-growing species adapted to resource-rich environments. Consequently, enemy release and increases in resource availability may act synergistically to favor exotic over native species.     

Macroevolutionary chemical escalation in an ancient plant–herbivore arms race

A central paradigm in the field of plant–herbivore interactions is that the diversity and complexity of secondary compounds in plants have intensified over evolutionary time, resulting in the great variety of secondary products that currently exists. Unfortunately, testing of this proposal has been very limited. We analyzed the volatile chemistry of 70 species of the tropical plant genus Bursera and used a molecular phylogeny to test whether the species'' chemical diversity or complexity have escalated. The results confirm that as new species diverged over time they tended to be armed not only with more compounds/species, but also with compounds that could potentially be more difficult for herbivores to adapt to because they belong to an increasing variety of chemical pathways. Overall chemical diversity in the genus also increased, but not as fast as species diversity, possibly because of allopatric species gaining improved defense with compounds that are new locally, but already in existence elsewhere.     

Tradeoffs associated with constitutive and induced plant resistance against herbivory

Several prominent hypotheses have been posed to explain the immense variability among plant species in defense against herbivores. A major concept in the evolutionary ecology of plant defenses is that tradeoffs of defense strategies are likely to generate and maintain species diversity. In particular, tradeoffs between constitutive and induced resistance and tradeoffs relating these strategies to growth and competitive ability have been predicted. We performed three independent experiments on 58 plant species from 15 different plant families to address these hypotheses in a phylogenetic framework. Because evolutionary tradeoffs may be altered by human-imposed artificial selection, we used 18 wild plant species and 40 cultivated garden-plant species. Across all 58 plant species, we demonstrate a tradeoff between constitutive and induced resistance, which was robust to accounting for phylogenetic history of the species. Moreover, the tradeoff was driven by wild species and was not evident for cultivated species. In addition, we demonstrate that more competitive species-but not fast growing ones-had lower constitutive but higher induced resistance. Thus, our multispecies experiments indicate that the competition-defense tradeoff holds for constitutive resistance and is complemented by a positive relationship of competitive ability with induced resistance. We conclude that the studied genetically determined tradeoffs are indeed likely to play an important role in shaping the high diversity observed among plant species in resistance against herbivores and in life history traits.     

Gene genealogies and population variation in plants

Early in the development of plant evolutionary biology, genetic drift, fluctuations in population size, and isolation were identified as critical processes that affect the course of evolution in plant species. Attempts to assess these processes in natural populations became possible only with the development of neutral genetic markers in the 1960s. More recently, the application of historically ordered neutral molecular variation (within the conceptual framework of coalescent theory) has allowed a reevaluation of these microevolutionary processes. Gene genealogies trace the evolutionary relationships among haplotypes (alleles) with populations. Processes such as selection, fluctuation in population size, and population substructuring affect the geographical and genealogical relationships among these alleles. Therefore, examination of these genealogical data can provide insights into the evolutionary history of a species. For example, studies of Arabidopsis thaliana have suggested that this species underwent rapid expansion, with populations showing little genetic differentiation. The new discipline of phylogeography examines the distribution of allele genealogies in an explicit geographical context. Phylogeographic studies of plants have documented the recolonization of European tree species from refugia subsequent to Pleistocene glaciation, and such studies have been instructive in understanding the origin and domestication of the crop cassava. Currently, several technical limitations hinder the widespread application of a genealogical approach to plant evolutionary studies. However, as these technical issues are solved, a genealogical approach holds great promise for understanding these previously elusive processes in plant evolution.     

Selection for chemical trait remixing in an invasive weed after reassociation with a coevolved specialist

The interaction between Depressaria pastinacella (parsnip webworm) and wild parsnip (Pastinaca sativa), in its native Europe and in its longstanding nonindigenous range in the midwestern United States, is characterized by chemical phenotype matching, ostensibly mediated by reciprocal selective responses. The first appearance of D. pastinacella on P. sativa in New Zealand in 2004 provided an opportunity to quantify selective impacts of a coevolved herbivore and calibrate rates of phytochemical response in its host plant. Webworms in 2006 reduced seed production up to 75% in New Zealand populations, and in 2007 infestations increased in severity in all populations except one. Most New Zealand populations fall into a furanocoumarin phenotype cluster distinct from European and U.S. phenotypes, although one heavily attacked population clusters with two U.S. populations and one European population long associated with webworms. Multivariate selection analysis substituting realized fitness (with webworms present) for potential fitness (absent webworms) as the dependent variable revealed that reassociation with a coevolved specialist in a nonindigenous area profoundly altered the selection regime, favoring trait remixing and rapid chemical changes in parsnip populations, as predicted by the geographic mosaic theory. That uninfested populations of New Zealand parsnips contain higher amounts of octyl acetate, a floral volatile used by webworms for orientation, suggests that plants that escape from specialized enemies may also experience selection to increase kairomones, as well as to reduce allomones.     

Cryptic sex and many-to-one coevolution in the fungus-growing ant symbiosis

The fungus-growing ants have long provided a spectacular example of coevolutionary integration. Their ecological success is thought to depend largely on the evolutionary alignment of reproductive interests between ants and fungi after vertical transmission and the ancient suppression of fungal sexuality. In the present study we test these assumptions and provide the first evidence of recombination in attine cultivars, contradicting widely held perceptions of obligate clonality. In addition, we document long-distance horizontal transmission of symbionts between leaf-cutter ant species on mainland Central America and South America and those endemic to Cuba, suggesting both lack of pairwise coevolutionary specificity in ant/cultivar interactions and dispersal of symbionts independent of their ant hosts. The coevolution between leaf-cutters and their fungal symbionts is thus not reciprocally pairwise. Rather, a single widespread and sexual fungal symbiont species is engaged in multiple interactions with divergent ant lineages. Strict fungal clonality and vertical transmission evidently have not played a critical role in the long-term evolutionary or ecological success of this well known mutualism.