Edward Allen Herre

Fungal endophytes limit pathogen damage in a tropical tree

Every plant species examined to date harbors endophytic fungi within its asymptomatic aerial tissues, such that endophytes represent a ubiquitous, yet cryptic, component of terrestrial plant communities. Fungal endophytes associated with leaves of woody angiosperms are especially diverse; yet, fundamental aspects of their interactions with hosts are unknown. In contrast to the relatively species-poor endophytes that are vertically transmitted and act as defensive mutualists of some temperate grasses, the diverse, horizontally transmitted endophytes of woody angiosperms are thought to contribute little to host defense. Here, we document high diversity, spatial structure, and host affinity among foliar endophytes associated with a tropical tree (Theobroma cacao, Malvaceae) across lowland Panama. We then show that inoculation of endophyte-free leaves with endophytes isolated frequently from naturally infected, asymptomatic hosts significantly decreases both leaf necrosis and leaf mortality when T. cacao seedlings are challenged with a major pathogen (Phytophthora sp.). In contrast to reports of fungal inoculation inducing systemic defense, we found that protection was primarily localized to endophyte-infected tissues. Further, endophyte-mediated protection was greater in mature leaves, which bear less intrinsic defense against fungal pathogens than do young leaves. In vitro studies suggest that host affinity is mediated by leaf chemistry, and that protection may be mediated by direct interactions of endophytes with foliar pathogens. Together, these data demonstrate the capacity of diverse, horizontally transmitted endophytes of woody angiosperms to play an important but previously unappreciated role in host defense.

Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest.

Negative density-dependent recruitment of seedlings, that is, seeds of a given species are less likely to become established seedlings if the density of that species is high, has been proposed to be an important mechanism contributing to the extraordinary diversity of tropical tree communities because it can potentially prevent any particular species from usurping all available space, either in close proximity to seed sources or at relatively larger spatial scales. However, density-dependent recruitment does not necessarily enhance community diversity. Furthermore, although density-dependent effects have been found at some life stages in some species, no study has shown that density-dependent recruitment affects community diversity. Here we report the results of observations in a lowland, moist forest in the Republic of Panamá in which the species identities of 386,027 seeds that arrived at 200 seed traps were compared with the species identities of 13,068 seedlings that recruited into adjacent plots over a 4-year period. Across the 200 sites, recruit seedling diversity was significantly higher than seed diversity. Part of this difference was explained by interspecies differences in average recruitment success. Even after accounting for these differences, however, negative density-dependent recruitment contributes significantly to the increase in diversity from seeds to seedling recruits.

The evolution of mutualisms: exploring the paths between conflict and cooperation

Mutualisms are of fundamental importance in all ecosystems but their very existence poses a series of challenging evolutionary questions. Recently, the application of molecular analyses combined with theoretical advances have transformed our understanding of many specific systems, thereby contributing to the possibility of a more general understanding of the factors that influence mutualisms.

Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest

The accumulation of species-specific enemies around adults is hypothesized to maintain plant diversity by limiting the recruitment of conspecific seedlings relative to heterospecific seedlings. Although previous studies in forested ecosystems have documented patterns consistent with the process of negative feedback, these studies are unable to address which classes of enemies (for example, pathogens, invertebrates, mammals) exhibit species-specific effects strong enough to generate negative feedback, and whether negative feedback at the level of the individual tree is sufficient to influence community-wide forest composition. Here we use fully reciprocal shade-house and field experiments to test whether the performance of conspecific tree seedlings (relative to heterospecific seedlings) is reduced when grown in the presence of enemies associated with adult trees. Both experiments provide strong evidence for negative plant–soil feedback mediated by soil biota. In contrast, above-ground enemies (mammals, foliar herbivores and foliar pathogens) contributed little to negative feedback observed in the field. In both experiments, we found that tree species that showed stronger negative feedback were less common as adults in the forest community, indicating that susceptibility to soil biota may determine species relative abundance in these tropical forests. Finally, our simulation models confirm that the strength of local negative feedback that we measured is sufficient to produce the observed community-wide patterns in tree-species relative abundance. Our findings indicate that plant–soil feedback is an important mechanism that can maintain species diversity and explain patterns of tree-species relative abundance in tropical forests.

Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest

We have used molecular techniques to investigate the diversity and distribution of the arbuscular mycorrhizal (AM) fungi colonizing tree seedling roots in the tropical forest on Barro Colorado Island (BCI), Republic of Panama. In the first year, we sampled newly emergent seedlings of the understory treelet Faramea occidentalis and the canopy emergent Tetragastris panamensis, from mixed seedling carpets at each of two sites. The following year we sampled surviving seedlings from these cohorts. The roots of 48 plants were analysed using AM fungal‐specific primers to amplify and clone partial small subunit (SSU) ribosomal RNA gene sequences. Over 1300 clones were screened for random fragment length polymorphism (RFLP) variation and 7% of these were sequenced. Compared with AM fungal communities sampled from temperate habitats using the same method, the overall diversity was high, with a total of 30 AM fungal types identified. Seventeen of these types have not been recorded previously, with the remainder being similar to types reported from temperate habitats. The tropical mycorrhizal population showed significant spatial heterogeneity and nonrandom associations with the different hosts. Moreover there was a strong shift in the mycorrhizal communities over time. AM fungal types that were dominant in the newly germinated seedlings were almost entirely replaced by previously rare types in the surviving seedlings the following year. The high diversity and huge variation detected across time points, sites and hosts, implies that the AM fungal types are ecologically distinct and thus may have the potential to influence recruitment and host composition in tropical forests.

Population structure and the evolution of virulence in nematode parasites of fig wasps.

It is often assumed that parasitic and disease-producing organisms tend to evolve benign relationships with their hosts over time. In contrast, theoretical arguments suggest that increased opportunities for parasite transmission will promote the evolution of increased virulence. The natural history of species-specific nematodes that parasitize fig-pollinating wasps permits the testing of these predictions in natural populations. For 11 species of Panamanian fig wasps, those species characterized by population structures that result in increased opportunities for parasite transmission harbor more virulent species of nematodes. In addition, differences in population structure are also associated with differences in other intra- and interspecific phenomena, including sex ratios among the fig wasp species, the degree of tension in the wasp-fig mutualism, and lethal combat among the males of parasitic wasps.

Sex Ratio Adjustment in Fig Wasps

The effects of inbreeding and local mate competition have often been confounded in theoretical and empirical studies of sex ratio. A general model considering the interplay of their influences on sex ratio evolution is presented, and its predictions are compared with data collected from three fig wasp species. The results indicate that female fig wasps adjust the sex ratio of their offspring in response to both the intensity of proximate local mate competition and the level of inbreeding in the population.

Cryptic species of fig-pollinating wasps: Implications for the evolution of the fig–wasp mutualism, sex allocation, and precision of adaptation

Fig-pollinating wasps have provided model systems for developing and testing theories of the evolution of mutualism, sex allocation, and precision of adaptation. With few exceptions, previous studies have assumed one species of pollinator wasp per host fig species. Here we report genetic data demonstrating the coexistence of previously undetected cryptic fig wasp species in at least half of the host fig species surveyed. The substantial mitochondrial sequence differences (4.2–6.1%) imply old divergences (≈1.5–5.1 million years ago) among these species. Furthermore, some cryptic species pairs seem to be sister taxa, whereas others clearly are not, indicating both long-term coexistence on shared hosts and the colonization of novel fig species. These findings undermine the prevalent notion of strict one-to-one specificity between cospeciating figs and their pollinators, thereby challenging existing theory concerning the evolution and stability of mutualisms. Moreover, the incorporation of the genetic information significantly improves the fit of the observed sex ratios to predictions of local mate-competition theory, further strengthening support for sex allocation theory and the precision of adaptation.

Testing Hamilton's rule with competition between relatives

Hamilton’s theory of kin selection suggests that individuals should show less aggression, and more altruism, towards closer kin. Recent theoretical work has, however, suggested that competition between relatives can counteract kin selection for altruism. Unfortunately, factors that tend to increase the average relatedness of interacting individuals—such as limited dispersal—also tend to increase the amount of competition between relatives. Therefore, in most natural systems, the conflicting influences of increased competition and increased relatedness are confounded, limiting attempts to test theory. Fig wasp taxa exhibit varying levels of aggression among non-dispersing males that show a range of average relatedness levels. Thus, across species, the effects of relatedness and competition between relatives can be separated. Here we report that—contrary to Hamiltons original prediction but in agreement with recent theory—the level of fighting between males shows no correlation with the estimated relatedness of interacting males, but is negatively correlated with future mating opportunities.

Coevolution of reproductive characteristics in 12 species of New World figs and their pollinator wasps

1) Figs (Ficus) and fig-pollination wasps (Agaonidae) are highly coevolved mutualists that depend completely on each other for continued reproduction. However, their reproductive interests are not identical. 2) The natural history of their interaction often permits the direct measurement of total lifetime reproductive success of the wasp and of major components of reproductive success for the fig. 3) Data from 12 monoecious species of New World figs (subgenusUrostigma) and their wasp pollinators (Pegoscapus spp.) indicate that fig fruit size (number of flowers per fruit), wasp size, and the number of foundresses that pollinate and lay eggs in any given fruit interact in complex but systematic ways to affect the reproductive success of both the wasps and the figs. 4) Different aspects of the interaction may work against the reproductive interests of either the wasp or the fig, or often, both. For example, in some species an ‘average’ foundress may only realize 25% of its reproductive potential due to the high average number of foundresses. However, that same crowding slects for more male-biased sex ratios in the wasps that reduce potential fitness gains through pollen dispersal for the fig. Nonetheless, the natural distributions of numbers of foundresses per fruit more clearly reflect the reproductive interests of the figs than of the wasps. 5) Generally, it appears that most of the fig species studied can be arranged along a continuum from those with physically small fruits that produce a relatively low proportion of viable seed butt are very efficient at the production of female wasps to physically large, relatively seed-rich fruits that are relatively inefficient at producing female wasps. The implications of these findings for the coevolution of figs and their wasps are discussed. Figs (Ficus) and fig-pollination wasps (Agaonidae) are highly coevolved mutualists that depend completely on each other for continued reproduction. However, their reproductive interests are not identical. The natural history of their interaction often permits the direct measurement of total lifetime reproductive success of the wasp and of major components of reproductive success for the fig. Data from 12 monoecious species of New World figs (subgenusUrostigma) and their wasp pollinators (Pegoscapus spp.) indicate that fig fruit size (number of flowers per fruit), wasp size, and the number of foundresses that pollinate and lay eggs in any given fruit interact in complex but systematic ways to affect the reproductive success of both the wasps and the figs. Different aspects of the interaction may work against the reproductive interests of either the wasp or the fig, or often, both. For example, in some species an ‘average’ foundress may only realize 25% of its reproductive potential due to the high average number of foundresses. However, that same crowding slects for more male-biased sex ratios in the wasps that reduce potential fitness gains through pollen dispersal for the fig. Nonetheless, the natural distributions of numbers of foundresses per fruit more clearly reflect the reproductive interests of the figs than of the wasps. Generally, it appears that most of the fig species studied can be arranged along a continuum from those with physically small fruits that produce a relatively low proportion of viable seed butt are very efficient at the production of female wasps to physically large, relatively seed-rich fruits that are relatively inefficient at producing female wasps. The implications of these findings for the coevolution of figs and their wasps are discussed.