The fig and pollinator wasp obligate mutualism is diverse (~750 described species), ecologically ... more The fig and pollinator wasp obligate mutualism is diverse (~750 described species), ecologically important, and ancient (~80-90 Ma), providing model systems for generating and testing many questions in evolution and ecology. Once thought to be a prime example of strict one-to-one cospeciation, current thinking suggests that genera of pollinator wasps coevolve with corresponding subsections of figs, but the degree to which cospeciation or other processes contributes to the association at finer scales is unclear. Here we use genome-wide sequence data from a community of Panamanian strangler figs (Ficus subgenus Urostigma, section Americana) and associated fig wasp pollinators (Pegoscapus spp.) to infer the process of coevolutionary diversification in this obligate mutualism. Using a model-based approach adapted from the study of gene family evolution, our results indicate pervasive and ongoing host switching of pollinator wasps at this fine phylogenetic and regional scale. Although th...
Inhomogeneities near the core-mantle boundary inferred from shortperiod scattered PKP waves recor... more Inhomogeneities near the core-mantle boundary inferred from shortperiod scattered PKP waves recorded at the global digital seismograph network.
SUMMARYThe natural history of fig-pollinating wasps and their associated species-specific nematod... more SUMMARYThe natural history of fig-pollinating wasps and their associated species-specific nematodes allows the measurement of many parameters which are relevant to testing hypotheses concerning host-parasite ecology and evolution. Within fig wasps species, it is possible to estimate lifetime reproductive success of foundress wasps as a function of presence or absence of nematode parasitism (virulence). Across species, there is a wide range of host population structures which, in turn, results in a range of opportunities for either horizontal or vertical nematode transmission. Therefore, estimates of virulence can be related to opportunities for transmission across a group of closely related hosts and their parasites. Further, the dynamics of the nematode infections over ecological and short-term evolutionary timescales can be monitored, giving added insight into the interpretation of the virulence estimates. Moreover, several scales of longer term evolutionary relationships are eith...
Active pollination, although rare, has been documented in a few pollination mutualisms. Such beha... more Active pollination, although rare, has been documented in a few pollination mutualisms. Such behaviour can only evolve if it benefits the pollinator in some way. The wasps that pollinate Ficus inflorescences can be active or passive pollinators. They lay their eggs in fig flowers, so that a proportion of flowers will host a wasp larva instead of a seed. We show in an actively pollinated monoecious fig that lack of pollination does not induce fig abortion or affect wasp offspring size but results in smaller numbers of offspring. Hence, conversely to other active pollination systems, seed formation is not obligatory to sustain developing pollinator larvae; however there is a direct fitness cost to active pollinators not to pollinate. We then compared the locations of eggs and fertilised flowers of three actively pollinated Ficus species and one passively pollinated species. We found that more flowers containing wasp eggs were fertilised in the actively pollinated species relative to those of the passively pollinated one. These results along with comparison with similar studies on dioecious figs, support the hypothesis that active pollination has evolved in fig wasps to ensure that more flowers containing wasp eggs are fertilised as this may increase the chances of successful gall development. The stigmatic platform characterising actively pollinated figs is probably an adaptation to increase pollen dispersion within the fig.
Abstract For 18 species of Panamanian Ficus, representing both basal (Pharmacosycea; 4 spp.) and ... more Abstract For 18 species of Panamanian Ficus, representing both basal (Pharmacosycea; 4 spp.) and derived (Urostigma, Americana; 14 spp.) sections, we sampled multiple individuals per species and analyzed sequence data from multiple (3) genetic markers (tpi, g3pdh, ...
The following species of the hereby redefined genus Parasitodiplogaster are described from fruits... more The following species of the hereby redefined genus Parasitodiplogaster are described from fruits of Ficus spp. in Panama : P.
Parasitodiplogaster species associated with Ficus maxima were surveyed at the Smithsonian Tropica... more Parasitodiplogaster species associated with Ficus maxima were surveyed at the Smithsonian Tropical Research Institute, Barro Colorado Island, Panama. Phase B-D syconia were collected from different trees and dissected in distilled water. Because there were different nematode stomatal and male morphotypes observed in a single sycone, nematodes isolated from each fig were observed to determine general morphotype class and stored individually in DNA extraction buffer for accurate morpho/molecular pairing. Additional voucher nematodes were gently heat-treated and fixed in formalin and processed into permanent mounts in dehydrated glycerin for more rigorous morphological examination. The survey yielded two different Parasitodiplogaster species: P. maxinema and P. pharmaconema n. sp. Several morphological characters, e.g., two long and stick-like teeth in the metastegostom, and stomatal dimorphism (presence of eurystomatous form) which were not previously described, were observed in P. maxinema and are ascribed hereto this species. Parasitodiplogaster pharmaconema n. sp. is morphologically similar to P. maxinema and P. yoponema but can be distinguished from these species based upon stomatal morphology, spicule and gubernaculum morphology, and number and arrangement of male genital papillae.
The following species of the hereby redefined genus Parasitodiplogaster are described from fruits... more The following species of the hereby redefined genus Parasitodiplogaster are described from fruits of Ficus spp. in Panama : P.
It is increasingly recognized that macro-organisms (corals, insects, plants, vertebrates) consist... more It is increasingly recognized that macro-organisms (corals, insects, plants, vertebrates) consist of both host tissues and multiple microbial symbionts that play essential roles in their host's ecological and evolutionary success. Consequently, identifying benefits and costs of symbioses, as well as mechanisms underlying them are research priorities. All plants surveyed under natural conditions harbor foliar endophytic fungi (FEF) in their leaf tissues, often at high densities. Despite producing no visible effects on their hosts, experiments have nonetheless shown that FEF reduce pathogen and herbivore damage. Here, combining results from three genomic, and two physiological experiments, we demonstrate pervasive genetic and phenotypic effects of the apparently asymptomatic endophytes on their hosts. Specifically, inoculation of endophyte-free (E−) Theobroma cacao leaves with Colletotrichum tropicale (E+), the dominant FEF species in healthy T. cacao, induces consistent changes in the expression of hundreds of host genes, including many with known defensive functions. Further, E+ plants exhibited increased lignin and cellulose content, reduced maximum rates of photosynthesis (A max), and enrichment of nitrogen-15 and carbon-13 isotopes. These phenotypic changes observed in E+ plants correspond to changes in expression of specific functional genes in related pathways. Moreover, a cacao gene (Tc00g04254) highly up-regulated by C. tropicale also confers resistance to pathogen damage in the absence of endophytes or their products in host tissues. Thus, the benefits of increased pathogen resistance in E+ plants are derived in part from up-regulation of intrinsic host defense responses, and appear to be offset by potential costs including reduced photosynthesis, altered host nitrogen metabolism, and endophyte heterotrophy of host tissues. Similar effects are likely in most plant-endophyte interactions, and should be recognized in the design and interpretation of genetic and phenotypic studies of plants.
To obtain tools for the estimation of inbreeding and assignment of offspring to matrilines, we de... more To obtain tools for the estimation of inbreeding and assignment of offspring to matrilines, we developed 13 microsatellite loci from the fig wasps that pollinate Ficus obtusifolia. Based on morphological studies, it was thought that a single species (Pegoscapus hoffmeyeri) pollinated this fig. However, our data revealed the presence of two coexisting cryptic species. Several diagnostic microsatellite markers may be used to distinguish these two cryptic species. The new microsatellites can be used across a wide range of fig-pollinating wasp species for both evolutionary and population genetic studies.
Wind-borne pollinating wasps (Agaonidae) can transport fig (Ficus sp., Moraceae) pollen over enor... more Wind-borne pollinating wasps (Agaonidae) can transport fig (Ficus sp., Moraceae) pollen over enormous distances (> 100 km). Because of their extensive breeding areas, Neotropical figs are expected to exhibit weak patterns of genetic structure at local and regional scales. We evaluated genetic structure at the regional to continental scale (Panama, Costa Rica, and Peru) for the free-standing fig species Ficus insipida. Genetic differentiation was detected only at distances > 300 km (Jost´s D est = 0.68 ± 0.07 & F ST = 0.30 ± 0.03 between Mesoamerican and Amazonian sites) and evidence for phylogeographic structure (R ST >>permuted R ST) was only significant in comparisons between Central and South America. Further, we assessed local scale spatial genetic structure (SGS, d 8 km) in Panama and developed an agent-based model parameterized with data from F. insipida to estimate minimum pollination distances, which determine the contribution of pollen dispersal on SGS. The local scale data for F. insipida was compared to SGS data collected for an additional free-standing fig, F. yoponensis (subgenus Pharmacosycea), and two species of strangler figs, F. citrifolia and F. obtusifolia (subgenus Urostigma) sampled in Panama. All four species displayed significant SGS (mean Sp = 0.014 ± 0.012). Model simulations indicated that most pollination events likely occur at distances > > 1 km, largely ruling out spatially limited pollen dispersal as the determinant of SGS in F. insipida and, by extension, the other fig species. Our results are consistent with the view that Ficus develops fine-scale SGS primarily as a result of localized seed dispersal and/or clumped seedling establishment despite extensive long-distance pollen dispersal. We discuss several ecological and life history factors that could have species-or subgenus-specific impacts on the genetic structure of Neotropical figs.
Ticks are important vectors of emerging zoonotic diseases. While adults of many tick species para... more Ticks are important vectors of emerging zoonotic diseases. While adults of many tick species parasitize mammals, immature ticks are often found on wild birds. In the tropics, difficulties in species-level identification of immature ticks hinder studies of tick ecology and tick-borne disease transmission, including any potential role for birds. In Panama, we found immature ticks on 227 out of 3,498 birds representing 93 host species, about 1/8th of the entire Panamanian terrestrial avifauna. Tick parasitism rates did not vary with temperature or rainfall, but parasitism rates did vary with host ecological traits: non-migratory residents, forest dwelling birds, bark insectivores, terrestrial foragers and lowland species were most likely to be infested with ticks. Using a molecular library developed from adult ticks specifically for this study, we identified 130 immature ticks obtained from wild birds, corresponding to eleven tick species, indicating that a substantial portion of the P...
Syconia (enclosed infructescences) infested with host-specific species of Schistonchus (Aphelench... more Syconia (enclosed infructescences) infested with host-specific species of Schistonchus (Aphelenchoididae) were collected from six species of Ficus (Moraceae) native to Florida or Panama. They were sectioned and histologically examined to assess the effects of parasitism. Parasitism by Schistonchus spp. was associated with hypertrophied cells, tissue necrosis, and the presence of an exudate in all species. Occasional hypertrophy of the outer epidermal cells occurred on seed florets, wasp florets, and on the endothecial cells of male florets in F. aurea (subgenus Urostigma) from Florida. Aberrations of the inner mesocarp occurred under the hypertrophied cells on seed florets. In F. laevigata (subgenus Urostigma) from Florida, Schistonchus sp. infested immature male florets and was associated with hypertrophy of endothecial cells, epidermal cells of the anther filaments, and anthers. Schistonchus sp. also caused aberrations of the anther filament, anthers, and pollen. Ficus poponoei (s...
Mutualisms are of fundamental importance in all ecosystems but their very existence poses a serie... more 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.
The fig and pollinator wasp obligate mutualism is diverse (~750 described species), ecologically ... more The fig and pollinator wasp obligate mutualism is diverse (~750 described species), ecologically important, and ancient (~80-90 Ma), providing model systems for generating and testing many questions in evolution and ecology. Once thought to be a prime example of strict one-to-one cospeciation, current thinking suggests that genera of pollinator wasps coevolve with corresponding subsections of figs, but the degree to which cospeciation or other processes contributes to the association at finer scales is unclear. Here we use genome-wide sequence data from a community of Panamanian strangler figs (Ficus subgenus Urostigma, section Americana) and associated fig wasp pollinators (Pegoscapus spp.) to infer the process of coevolutionary diversification in this obligate mutualism. Using a model-based approach adapted from the study of gene family evolution, our results indicate pervasive and ongoing host switching of pollinator wasps at this fine phylogenetic and regional scale. Although th...
Inhomogeneities near the core-mantle boundary inferred from shortperiod scattered PKP waves recor... more Inhomogeneities near the core-mantle boundary inferred from shortperiod scattered PKP waves recorded at the global digital seismograph network.
SUMMARYThe natural history of fig-pollinating wasps and their associated species-specific nematod... more SUMMARYThe natural history of fig-pollinating wasps and their associated species-specific nematodes allows the measurement of many parameters which are relevant to testing hypotheses concerning host-parasite ecology and evolution. Within fig wasps species, it is possible to estimate lifetime reproductive success of foundress wasps as a function of presence or absence of nematode parasitism (virulence). Across species, there is a wide range of host population structures which, in turn, results in a range of opportunities for either horizontal or vertical nematode transmission. Therefore, estimates of virulence can be related to opportunities for transmission across a group of closely related hosts and their parasites. Further, the dynamics of the nematode infections over ecological and short-term evolutionary timescales can be monitored, giving added insight into the interpretation of the virulence estimates. Moreover, several scales of longer term evolutionary relationships are eith...
Active pollination, although rare, has been documented in a few pollination mutualisms. Such beha... more Active pollination, although rare, has been documented in a few pollination mutualisms. Such behaviour can only evolve if it benefits the pollinator in some way. The wasps that pollinate Ficus inflorescences can be active or passive pollinators. They lay their eggs in fig flowers, so that a proportion of flowers will host a wasp larva instead of a seed. We show in an actively pollinated monoecious fig that lack of pollination does not induce fig abortion or affect wasp offspring size but results in smaller numbers of offspring. Hence, conversely to other active pollination systems, seed formation is not obligatory to sustain developing pollinator larvae; however there is a direct fitness cost to active pollinators not to pollinate. We then compared the locations of eggs and fertilised flowers of three actively pollinated Ficus species and one passively pollinated species. We found that more flowers containing wasp eggs were fertilised in the actively pollinated species relative to those of the passively pollinated one. These results along with comparison with similar studies on dioecious figs, support the hypothesis that active pollination has evolved in fig wasps to ensure that more flowers containing wasp eggs are fertilised as this may increase the chances of successful gall development. The stigmatic platform characterising actively pollinated figs is probably an adaptation to increase pollen dispersion within the fig.
Abstract For 18 species of Panamanian Ficus, representing both basal (Pharmacosycea; 4 spp.) and ... more Abstract For 18 species of Panamanian Ficus, representing both basal (Pharmacosycea; 4 spp.) and derived (Urostigma, Americana; 14 spp.) sections, we sampled multiple individuals per species and analyzed sequence data from multiple (3) genetic markers (tpi, g3pdh, ...
The following species of the hereby redefined genus Parasitodiplogaster are described from fruits... more The following species of the hereby redefined genus Parasitodiplogaster are described from fruits of Ficus spp. in Panama : P.
Parasitodiplogaster species associated with Ficus maxima were surveyed at the Smithsonian Tropica... more Parasitodiplogaster species associated with Ficus maxima were surveyed at the Smithsonian Tropical Research Institute, Barro Colorado Island, Panama. Phase B-D syconia were collected from different trees and dissected in distilled water. Because there were different nematode stomatal and male morphotypes observed in a single sycone, nematodes isolated from each fig were observed to determine general morphotype class and stored individually in DNA extraction buffer for accurate morpho/molecular pairing. Additional voucher nematodes were gently heat-treated and fixed in formalin and processed into permanent mounts in dehydrated glycerin for more rigorous morphological examination. The survey yielded two different Parasitodiplogaster species: P. maxinema and P. pharmaconema n. sp. Several morphological characters, e.g., two long and stick-like teeth in the metastegostom, and stomatal dimorphism (presence of eurystomatous form) which were not previously described, were observed in P. maxinema and are ascribed hereto this species. Parasitodiplogaster pharmaconema n. sp. is morphologically similar to P. maxinema and P. yoponema but can be distinguished from these species based upon stomatal morphology, spicule and gubernaculum morphology, and number and arrangement of male genital papillae.
The following species of the hereby redefined genus Parasitodiplogaster are described from fruits... more The following species of the hereby redefined genus Parasitodiplogaster are described from fruits of Ficus spp. in Panama : P.
It is increasingly recognized that macro-organisms (corals, insects, plants, vertebrates) consist... more It is increasingly recognized that macro-organisms (corals, insects, plants, vertebrates) consist of both host tissues and multiple microbial symbionts that play essential roles in their host's ecological and evolutionary success. Consequently, identifying benefits and costs of symbioses, as well as mechanisms underlying them are research priorities. All plants surveyed under natural conditions harbor foliar endophytic fungi (FEF) in their leaf tissues, often at high densities. Despite producing no visible effects on their hosts, experiments have nonetheless shown that FEF reduce pathogen and herbivore damage. Here, combining results from three genomic, and two physiological experiments, we demonstrate pervasive genetic and phenotypic effects of the apparently asymptomatic endophytes on their hosts. Specifically, inoculation of endophyte-free (E−) Theobroma cacao leaves with Colletotrichum tropicale (E+), the dominant FEF species in healthy T. cacao, induces consistent changes in the expression of hundreds of host genes, including many with known defensive functions. Further, E+ plants exhibited increased lignin and cellulose content, reduced maximum rates of photosynthesis (A max), and enrichment of nitrogen-15 and carbon-13 isotopes. These phenotypic changes observed in E+ plants correspond to changes in expression of specific functional genes in related pathways. Moreover, a cacao gene (Tc00g04254) highly up-regulated by C. tropicale also confers resistance to pathogen damage in the absence of endophytes or their products in host tissues. Thus, the benefits of increased pathogen resistance in E+ plants are derived in part from up-regulation of intrinsic host defense responses, and appear to be offset by potential costs including reduced photosynthesis, altered host nitrogen metabolism, and endophyte heterotrophy of host tissues. Similar effects are likely in most plant-endophyte interactions, and should be recognized in the design and interpretation of genetic and phenotypic studies of plants.
To obtain tools for the estimation of inbreeding and assignment of offspring to matrilines, we de... more To obtain tools for the estimation of inbreeding and assignment of offspring to matrilines, we developed 13 microsatellite loci from the fig wasps that pollinate Ficus obtusifolia. Based on morphological studies, it was thought that a single species (Pegoscapus hoffmeyeri) pollinated this fig. However, our data revealed the presence of two coexisting cryptic species. Several diagnostic microsatellite markers may be used to distinguish these two cryptic species. The new microsatellites can be used across a wide range of fig-pollinating wasp species for both evolutionary and population genetic studies.
Wind-borne pollinating wasps (Agaonidae) can transport fig (Ficus sp., Moraceae) pollen over enor... more Wind-borne pollinating wasps (Agaonidae) can transport fig (Ficus sp., Moraceae) pollen over enormous distances (> 100 km). Because of their extensive breeding areas, Neotropical figs are expected to exhibit weak patterns of genetic structure at local and regional scales. We evaluated genetic structure at the regional to continental scale (Panama, Costa Rica, and Peru) for the free-standing fig species Ficus insipida. Genetic differentiation was detected only at distances > 300 km (Jost´s D est = 0.68 ± 0.07 & F ST = 0.30 ± 0.03 between Mesoamerican and Amazonian sites) and evidence for phylogeographic structure (R ST >>permuted R ST) was only significant in comparisons between Central and South America. Further, we assessed local scale spatial genetic structure (SGS, d 8 km) in Panama and developed an agent-based model parameterized with data from F. insipida to estimate minimum pollination distances, which determine the contribution of pollen dispersal on SGS. The local scale data for F. insipida was compared to SGS data collected for an additional free-standing fig, F. yoponensis (subgenus Pharmacosycea), and two species of strangler figs, F. citrifolia and F. obtusifolia (subgenus Urostigma) sampled in Panama. All four species displayed significant SGS (mean Sp = 0.014 ± 0.012). Model simulations indicated that most pollination events likely occur at distances > > 1 km, largely ruling out spatially limited pollen dispersal as the determinant of SGS in F. insipida and, by extension, the other fig species. Our results are consistent with the view that Ficus develops fine-scale SGS primarily as a result of localized seed dispersal and/or clumped seedling establishment despite extensive long-distance pollen dispersal. We discuss several ecological and life history factors that could have species-or subgenus-specific impacts on the genetic structure of Neotropical figs.
Ticks are important vectors of emerging zoonotic diseases. While adults of many tick species para... more Ticks are important vectors of emerging zoonotic diseases. While adults of many tick species parasitize mammals, immature ticks are often found on wild birds. In the tropics, difficulties in species-level identification of immature ticks hinder studies of tick ecology and tick-borne disease transmission, including any potential role for birds. In Panama, we found immature ticks on 227 out of 3,498 birds representing 93 host species, about 1/8th of the entire Panamanian terrestrial avifauna. Tick parasitism rates did not vary with temperature or rainfall, but parasitism rates did vary with host ecological traits: non-migratory residents, forest dwelling birds, bark insectivores, terrestrial foragers and lowland species were most likely to be infested with ticks. Using a molecular library developed from adult ticks specifically for this study, we identified 130 immature ticks obtained from wild birds, corresponding to eleven tick species, indicating that a substantial portion of the P...
Syconia (enclosed infructescences) infested with host-specific species of Schistonchus (Aphelench... more Syconia (enclosed infructescences) infested with host-specific species of Schistonchus (Aphelenchoididae) were collected from six species of Ficus (Moraceae) native to Florida or Panama. They were sectioned and histologically examined to assess the effects of parasitism. Parasitism by Schistonchus spp. was associated with hypertrophied cells, tissue necrosis, and the presence of an exudate in all species. Occasional hypertrophy of the outer epidermal cells occurred on seed florets, wasp florets, and on the endothecial cells of male florets in F. aurea (subgenus Urostigma) from Florida. Aberrations of the inner mesocarp occurred under the hypertrophied cells on seed florets. In F. laevigata (subgenus Urostigma) from Florida, Schistonchus sp. infested immature male florets and was associated with hypertrophy of endothecial cells, epidermal cells of the anther filaments, and anthers. Schistonchus sp. also caused aberrations of the anther filament, anthers, and pollen. Ficus poponoei (s...
Mutualisms are of fundamental importance in all ecosystems but their very existence poses a serie... more 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.
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