Host insect specificity and interspecific competition drive parasitoid diversification in a plant-insect community.

Ecological interactions among plants, insect herbivores, and parasitoids are pervasive in nature and play important roles in community assembling, but the codiversification of tri-trophic interactions has received less attention. Here we compare pairwise codiversification patterns between a set of 22 fig species, their herbivorous pollinating and galling wasps, and their parasitoids. The parasitoid phylogeny showed significant congruence and more cospeciation events with host insects phylogeny than with host plants. These results suggest that parasitoid phylogeny and speciation is more closely related to their host insects than to their host plants. The pollinating wasps hosted more parasitoid species than gallers and indicated a more intense interspecific competition among parasitoids associated with pollinators. Closer matching and fewer evolutionary host shifts were found between parasitoids and galler hosts than between parasitoids and pollinator hosts. These results suggest that interspecific competition among parasitoids, rather than resource availability of host wasps, is the main driver of the codiversification pattern in this community. Therefore, our study highlights the important role of interspecific competition among high trophic level insects in plant-insect tri-trophic community assembling.

Diversity begets diversity: Low resource heterogeneity reduces the diversity of nut-nesting ants in rubber plantations.

One of the most general patterns in ecology is the positive relationship between environmental heterogeneity and local diversity. On the one hand, increased resource heterogeneity provides more resources for diverse consumers in the community. On the other hand, increased structural heterogeneity creates variation in the environment's physical structure, thus allowing the coexistence of diverse species with different environmental requirements. Here, we examined the relative importance of resource and structural heterogeneity in determining the taxonomic, functional, and phylogenetic diversity of nut-nesting ants in natural rainforest and rubber plantation. The species richness of nut-nesting ants was 70% higher in rainforest than in rubber plantation. The clustered functional and phylogenetic structure in rubber plantation suggested a strong effect of environmental filtering in shaping ant functional and phylogenetic structure. Nesting heterogeneity (nut diversity) was the major factor explaining variation in taxonomic, functional, and phylogenetic diversity, suggesting that resource heterogeneity plays a major role in shaping the biodiversity patterns of nut-nesting ants. Overall, these results indicate that decreased resource diversity following the conversion of rainforest to rubber plantation can drive biodiversity loss in nut-nesting ants, through its effect on reducing both ant species, functional, and phylogenetic diversity. The decline in species richness and functional and phylogenetic diversity in the local ant community might have major effects on ecosystem functioning.

Climate and land-use interactively shape butterfly diversity in tropical rainforest and savanna ecosystems of southwestern China.

Human-induced habitat conversion and degradation, along with accelerating climatic change, have resulted in considerable global biodiversity loss. Nevertheless, how local ecological assemblages respond to the interplay between climate and land-use change remains poorly understood. Here, we examined the effects of climate and land-use interactions on butterfly diversity in different ecosystems of southwestern China. Specifically, we investigated variation in the alpha and beta diversities of butterflies in different landscapes along human-modified and climate gradients. We found that increasing land-use intensity not only caused a dramatic decrease in butterfly alpha diversity but also significantly simplified butterfly species composition in tropical rainforest and savanna ecosystems. These findings suggest that habitat modification by agricultural activities increases the importance of deterministic processes and leads to biotic homogenization. The land-use intensity model best explained species richness variation in the tropical rainforest, whereas the climate and land-use intensity interaction model best explained species richness variation in the savanna. These results indicate that climate modulates the effects of land-use intensity on butterfly alpha diversity in the savanna ecosystem. We also found that the response of species composition to climate varied between sites: specifically, species composition was strongly correlated with climatic distance in the tropical rainforest but not in the savanna. Taken together, our long-term butterfly monitoring data reveal that interactions between human-modified habitat change and climate change have shaped butterfly diversity in tropical rainforest and savanna. These findings also have important implications for biodiversity conservation under the current era of rapid human-induced habitat loss and climate change.

The nature of interspecific interactions and co-diversification patterns, as illustrated by the fig microcosm.

Interactions between mutualists, competitors, and antagonists have contrasting ecological effects that, sustained over generations, can influence micro- and macroevolution. Dissimilar benefits and costs for these interactions should cause contrasting co-diversification patterns between interacting clades, with prevalent co-speciation by mutualists, association loss by competitors, and host switching by antagonists. We assessed these expectations for a local assemblage of 26 fig species (Moraceae: Ficus), 26 species of mutualistic (pollinating), and 33 species of parasitic (galling) wasps (Chalcidoidea). Using newly acquired gene sequences, we inferred the phylogenies for all three clades. We then compared the three possible pairs of phylogenies to assess phylogenetic congruence and the relative frequencies of co-speciation, association duplication, switching, and loss. The paired phylogenies of pollinators with their mutualists and competitors were significantly congruent, unlike that of figs and their parasites. The distributions of macroevolutionary events largely agreed with expectations for mutualists and antagonists. By contrast, that for competitors involved relatively frequent association switching, as expected, but also unexpectedly frequent co-speciation. The latter result likely reflects the heterogeneous nature of competition among fig wasps. These results illustrate the influence of different interspecific interactions on co-diversification, while also revealing its dependence on specific characteristics of those interactions.

A comparative venomic fingerprinting approach reveals that galling and non-galling fig wasp species have different venom profiles.

The galling habit represents a complex type of interaction between insects and plants, ranging from antagonism to mutualism. The obligate pollination mutualism between Ficus and fig wasps relies strongly on the induction of galls in Ficus flowers, where wasps' offspring develop. Even though gall induction plays an important role in many insect-plant interactions, the mechanisms that trigger gall formation are still not completely known. Using a fingerprinting approach, we show here that venom protein profiles from galling fig wasps differ from the venom profiles of non-galling species, suggesting the secretion plays different roles according to the type of interaction it is involved in. Each studied cleptoparasitic species had a distinct venom profile, suggesting that cleptoparasitism in fig wasps covers a vast diversity of molecular interactions. Fig wasp venoms are mainly composed of peptides. No low molecular weight compounds were detected by UPLC-DAD-MS, suggesting that such compounds (e.g., IAA and cytokinines) are not involved in gall induction. The differences in venom composition observed between galling and non-galling fig wasp species bring new perspectives to the study of gall induction processes and the role of insect secretions.

Chemical camouflage: a key process in shaping an ant-treehopper and fig-fig wasp mutualistic network.

Different types of mutualisms may interact, co-evolve and form complex networks of interdependences, but how species interact in networks of a mutualistic community and maintain its stability remains unclear. In a mutualistic network between treehoppers-weaver ants and fig-pollinating wasps, we found that the cuticular hydrocarbons of the treehoppers are more similar to the surface chemical profiles of fig inflorescence branches (FIB) than the cuticular hydrocarbons of the fig wasps. Behavioral assays showed that the cuticular hydrocarbons from both treehoppers and FIBs reduce the propensity of weaver ants to attack treehoppers even in the absence of honeydew rewards, suggesting that chemical camouflage helps enforce the mutualism between weaver ants and treehoppers. High levels of weaver ant and treehopper abundances help maintain the dominance of pollinating fig wasps in the fig wasp community and also increase fig seed production, as a result of discriminative predation and disturbance by weaver ants of ovipositing non-pollinating fig wasps (NPFWs). Ants therefore help preserve this fig-pollinating wasp mutualism from over exploitation by NPFWs. Our results imply that in this mutualistic network chemical camouflage plays a decisive role in regulating the behavior of a key species and indirectly shaping the architecture of complex arthropod-plant interactions.

The caterpillar fungus, Ophiocordyceps sinensis, genome provides insights into highland adaptation of fungal pathogenicity.

To understand the potential genetic basis of highland adaptation of fungal pathogenicity, we present here the ~116 Mb de novo assembled high-quality genome of Ophiocordyceps sinensis endemic to the Qinghai-Tibetan Plateau. Compared with other plain-dwelling fungi, we find about 3.4-fold inflation of the O. sinensis genome due to a rapid amplification of long terminal repeat retrotransposons that occurred ~38 million years ago in concert with the uplift of the plateau. We also observe massive removal of thousands of genes related to the transport process and energy metabolism. O. sinensis displays considerable lineage-specific expansion of gene families functionally enriched in the adaptability of low-temperature of cold tolerance, fungal pathogenicity and specialized host infection. We detect signals of positive selection for genes involved in peroxidase and hypoxia to enable its highland adaptation. Resequencing and analyzing 31 whole genomes of O. sinensis, representing nearly all of its geographic range, exhibits latitude-based population divergence and nature selection for population inhabitation towards higher altitudes on the Qinghai-Tibetan Plateau.

Hepatitis C virus and antiviral innate immunity: who wins at tug-of-war?

Hepatitis C virus (HCV) is a major human pathogen of chronic hepatitis and related liver diseases. Innate immunity is the first line of defense against invading foreign pathogens, and its activation is dependent on the recognition of these pathogens by several key sensors. The interferon (IFN) system plays an essential role in the restriction of HCV infection via the induction of hundreds of IFN-stimulated genes (ISGs) that inhibit viral replication and spread. However, numerous factors that trigger immune dysregulation, including viral factors and host genetic factors, can help HCV to escape host immune response, facilitating viral persistence. In this review, we aim to summarize recent advances in understanding the innate immune response to HCV infection and the mechanisms of ISGs to suppress viral survival, as well as the immune evasion strategies for chronic HCV infection.

New records of ant species from Yunnan, China.

As with many other regions of the world, significant collecting, curation, and taxonomic efforts will be needed to complete the inventory of China's ant fauna. This is especially true for the highly diverse tropical regions in the south of the country, where moist tropical forests harbor high species richness typical of the Southeast Asian region. We inventoried ants in the Xingshuangbanna prefecture, Yunnan, in June 2013, using a variety of methods including Winkler extraction and hand collection to sample ant diversity. We identified 213 species/morphospecies of ants from 10 subfamilies and 61 genera. After identification of 148 valid species of the 213 total species collected, 40 species represent new records for Yunnan province and 17 species are newly recorded for China. This increases the total number of named ant species in Yunnan and China to 447 and 951 respectively. The most common species collected were Brachyponeraluteipes and Vollenhoviaemeryi. Only one confirmed exotic species Strumigenysmembranifera, was collected, although several others were potentially introduced by humans. These results highlight the high biodiversity value of the region, but also underscore how much work remains to fully document the native myrmecofauna.

The incidence and pattern of copollinator diversification in dioecious and monoecious figs.

Differences in breeding system are associated with correlated ecological and morphological changes in plants. In Ficus, dioecy and monoecy are strongly associated with different suites of traits (tree height, population density, fruiting frequency, pollinator dispersal ecology). Although approximately 30% of fig species are pollinated by multiple species of fig-pollinating wasps, it has been suggested that copollinators are rare in dioecious figs. Here, we test whether there is a connection between the fig breeding system and copollinator incidence and diversification by conducting a meta-analysis of molecular data from pollinators of 119 fig species that includes new data from 15 Asian fig species. We find that the incidence of copollinators is not significantly different between monoecious and dioecious Ficus. Surprisingly, while all copollinators in dioecious figs are sister taxa, only 32.1% in monoecious figs are sister taxa. We present hypotheses to explain those patterns and discuss their consequences on the evolution of this mutualism.

Has pollination mode shaped the evolution of ficus pollen?

BACKGROUND: The extent to which co-evolutionary processes shape morphological traits is one of the most fascinating topics in evolutionary biology. Both passive and active pollination modes coexist in the fig tree (Ficus, Moraceae) and fig wasp (Agaonidae, Hymenoptera) mutualism. This classic obligate relationship that is about 75 million years old provides an ideal system to consider the role of pollination mode shifts on pollen evolution. METHODS AND MAIN FINDINGS: Twenty-five fig species, which cover all six Ficus subgenera, and are native to the Xishuangbanna region of southwest China, were used to investigate pollen morphology with scanning electron microscope (SEM). Pollination mode was identified by the Anther/Ovule ratio in each species. Phylogenetic free regression and a correlated evolution test between binary traits were conducted based on a strong phylogenetic tree. Seventeen of the 25 fig species were actively pollinated and eight species were passively pollinated. Three pollen shape types and three kinds of exine ornamentation were recognized among these species. Pollen grains with ellipsoid shape and rugulate ornamentation were dominant. Ellipsoid pollen occurred in all 17 species of actively pollinated figs, while for the passively pollinated species, two obtuse end shapes were identified: cylinder and sphere shapes were identified in six of the eight species. All passively pollinated figs presented rugulate ornamentation, while for actively pollinated species, the smoother types - psilate and granulate-rugulate ornamentations - accounted for just five and two among the 17 species, respectively. The relationship between pollen shape and pollination mode was shown by both the phylogenetic free regression and the correlated evolution tests. CONCLUSIONS: Three pollen shape and ornamentation types were found in Ficus, which show characteristics related to passive or active pollination mode. Thus, the pollen shape is very likely shaped by pollination mode in this unique obligate mutualism.

Premature attraction of pollinators to inaccessible figs of Ficus altissima: a search for ecological and evolutionary consequences.

Adult life spans of only one or two days characterise life cycles of the fig wasps (Agaonidae) that pollinate fig trees (Ficus spp., Moraceae). Selection is expected to favour traits that maximise the value of the timing of encounters between such mutualistic partners, and fig wasps are usually only attracted to their hosts by species- and developmental-stage specific volatiles released from figs at the time when they are ready to be entered, oviposited in and pollinated. We found that Ficus altissima is exceptional, because it has persistent tight-fitting bud covers that prevent its Eupristina altissima pollinator (and a second species of 'cheater' agaonid) from entering its figs for several days after they start to be attracted. We examined the consequences of delayed entry for the figs and fig wasps and tested whether delayed entry has been selected to increase adult longevity. We found that older pollinators produced fewer and smaller offspring, but seed production was more efficient. Pollinator offspring ratios also varied depending on the age of figs they entered. The two agaonids from F. altissima lived slightly longer than six congeners associated with typical figs, but this was explainable by their larger body sizes. Delayed entry generates reproductive costs, especially for the pollinator. This opens an interesting perspective on the coevolution of figs and their pollinators and on the nature of mutualistic interactions in general.

Larger fig wasps are more careful about which figs to enter--with good reason.

Floral longevity reflects a balance between gains in pollinator visitation and the costs of flower maintenance. Because rewards to pollinators change over time, older flowers may be less attractive, reducing the value of extended longevity. Un-pollinated figs, the inflorescences of Ficus species, can remain receptive for long periods, but figs that are older when entered by their host-specific fig wasp pollinators produce fewer seeds and fig wasp offspring. Our field experiments with Ficushispida, a dioecious fig tree, examined how the length of time that receptive figs have remained un-pollinated influences the behaviour and reproductive success of its short-lived fig wasp pollinator, Ceratosolensolmsi marchali. The results were consistent in three different seasons, and on male and female trees, although receptivity was greatly extended during colder months. Pollinators took longer to find the ostioles of older figs, and longer to penetrate them. They also became increasingly unwilling to enter figs as they aged, and increasing numbers of the wasps became trapped in the ostiolar bracts. Larger individuals were particularly unwilling to enter older figs, resulting in older figs being pollinated by smaller wasps. On female trees, where figs produce only seeds, seed production declined rapidly with fig age. On male trees, the numbers and size of fig wasp offspring declined, and a higher proportion were male. Older male figs are harder to enter, especially for larger individuals, and offer poorer quality oviposition opportunities. This study opens an interesting new perspective on the coevolution of figs and their pollinators, especially factors influencing pollinator body size and emphasises the subtleties of interactions between mutualists.

Utilisation of chemical signals by inquiline wasps in entering their host figs.

The fig tree, Ficus curtipes, hosts an obligate pollinating wasp, an undescribed Eupristina sp., but can also be pollinated by two inquiline (living in the burrow, nest, gall, or other habitation of another animal) wasps, Diaziella yangi and an undescribed Lipothymus sp. The two inquilines are unable to independently induce galls and depend on the galls induced by the obligate pollinator for reproduction and, therefore, normally enter receptive F. curtipes figs colonised by the obligate pollinators. However, sometimes the inquilines also enter figs that are not colonised by the pollinators, despite consequent reproductive failure. It is still unknown which signal(s) the inquilines use in entering the colonised and non-colonised figs. We conducted behavioural experiments to investigate several possible signals utilised by the inquilines in entering their host receptive figs. Our investigation showed that both inquiline species enter the receptive F. curtipes figs in response to the body odours of the obligate wasps and one of the main compounds emitted by the figs, 6-methyl-5-hepten-2-one. The compound was not found in the pollinator body odours, suggesting that the two inquiline wasps can utilise two signals to enter their host figs, which is significant for the evolution of the fig-fig wasp system. These inquilines could evolve to become mutualists of the figs if they evolve the ability to independently gall fig flowers; there is, however, another possibility that a monoecious Ficus species hosting such inquilines may evolve into a dioecious one if these inquilines cannot evolve the above-mentioned ability. Additionally, this finding provides evidence for the evolution of chemical communication between plants and insects.

Rediscovery of the rare ant genus Bannapone (Hymenoptera: Formicidae: Amblyoponinae) and description of the worker caste.

The genus Bannapone was described in 2000 on the basis of a single dealate queen specimen. Since its original collection in Yunnan, China, no other specimen has been reported, making it one of the rarest ant genera in the world. Here we report the collection of two workers of Bannapone also from Yunnan province. The description of the worker caste is presented. Furthermore, we found significant differences with the described B. mulanae Xu, 2000 which leads us to describe the workers as a new species, B. scrobiceps n. sp.. Finally, we briefly discuss the importance of leaf-litter collection methods to collect taxa considered as "rare".

Description of two new species of Walkerella (Pteromalidae, Otitesellinae) from China with a key to species of the genus.

Walkerella is an Old World genus of non-pollinating fig wasps in the subfamily Otitesellinae (Chalcidoidea, Pteromalidae). It is the most widely distributed genus of the subfamily, though there has been only six known world species. This paper describes two new species associated with the host Ficus subsection Conosycea of section Urostigma, subgenus Urostigma in Xishuangbanna, China. The two new species, Walkerella nigrabdomina Ma & Yang sp. nov. and W. curtipedis Ma & Yang sp. nov., are described from specimens reared from Ficus pisocarpa and Ficus curtipes, respectively. A key to all described species of Walkerella found is provided.

An extreme case of plant-insect codiversification: figs and fig-pollinating wasps.

It is thought that speciation in phytophagous insects is often due to colonization of novel host plants, because radiations of plant and insect lineages are typically asynchronous. Recent phylogenetic comparisons have supported this model of diversification for both insect herbivores and specialized pollinators. An exceptional case where contemporaneous plant-insect diversification might be expected is the obligate mutualism between fig trees (Ficus species, Moraceae) and their pollinating wasps (Agaonidae, Hymenoptera). The ubiquity and ecological significance of this mutualism in tropical and subtropical ecosystems has long intrigued biologists, but the systematic challenge posed by >750 interacting species pairs has hindered progress toward understanding its evolutionary history. In particular, taxon sampling and analytical tools have been insufficient for large-scale cophylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on an average, wasps had sequences from 77% of 6 genes (5.6 kb), figs had sequences from 60% of 5 genes (5.5 kb), and overall 850 new DNA sequences were generated for this study. We also developed a new analytical tool, Jane 2, for event-based phylogenetic reconciliation analysis of very large data sets. Separate Bayesian phylogenetic analyses for figs and fig wasps under relaxed molecular clock assumptions indicate Cretaceous diversification of crown groups and contemporaneous divergence for nearly half of all fig and pollinator lineages. Event-based cophylogenetic analyses further support the codiversification hypothesis. Biogeographic analyses indicate that the present-day distribution of fig and pollinator lineages is consistent with a Eurasian origin and subsequent dispersal, rather than with Gondwanan vicariance. Overall, our findings indicate that the fig-pollinator mutualism represents an extreme case among plant-insect interactions of coordinated dispersal and long-term codiversification. [Biogeography; coevolution; cospeciation; host switching; long-branch attraction; phylogeny.].

The complete mitochondrial genomes of two ghost moths, Thitarodes renzhiensis and Thitarodes yunnanensis: the ancestral gene arrangement in Lepidoptera.

BACKGROUND: Lepidoptera encompasses more than 160,000 described species that have been classified into 45-48 superfamilies. The previously determined Lepidoptera mitochondrial genomes (mitogenomes) are limited to six superfamilies of the lineage Ditrysia. Compared with the ancestral insect gene order, these mitogenomes all contain a tRNA rearrangement. To gain new insights into Lepidoptera mitogenome evolution, we sequenced the mitogenomes of two ghost moths that belong to the non-ditrysian lineage Hepialoidea and conducted a comparative mitogenomic analysis across Lepidoptera. RESULTS: The mitogenomes of Thitarodes renzhiensis and T. yunnanensis are 16,173 bp and 15,816 bp long with an A + T content of 81.28 % and 82.34 %, respectively. Both mitogenomes include 13 protein-coding genes, 22 transfer RNA genes, 2 ribosomal RNA genes, and the A + T-rich region. Different tandem repeats in the A + T-rich region mainly account for the size difference between the two mitogenomes. All the protein-coding genes start with typical mitochondrial initiation codons, except for cox1 (CGA) and nad1 (TTG) in both mitogenomes. The anticodon of trnS(AGN) in T. renzhiensis and T. yunnanensis is UCU instead of the mostly used GCU in other sequenced Lepidoptera mitogenomes. The 1,584-bp sequence from rrnS to nad2 was also determined for an unspecified ghost moth (Thitarodes sp.), which has no repetitive sequence in the A + T-rich region. All three Thitarodes species possess the ancestral gene order with trnI-trnQ-trnM located between the A + T-rich region and nad2, which is different from the gene order trnM-trnI-trnQ in all previously sequenced Lepidoptera species. The formerly identified conserved elements of Lepidoptera mitogenomes (i.e. the motif 'ATAGA' and poly-T stretch in the A + T-rich region and the long intergenic spacer upstream of nad2) are absent in the Thitarodes mitogenomes. CONCLUSION: The mitogenomes of T. renzhiensis and T. yunnanensis exhibit unusual features compared with the previously determined Lepidoptera mitogenomes. Their ancestral gene order indicates that the tRNA rearrangement event(s) likely occurred after Hepialoidea diverged from other lepidopteran lineages. Characterization of the two ghost moth mitogenomes has enriched our knowledge of Lepidoptera mitogenomes and contributed to our understanding of the mechanisms underlying mitogenome evolution, especially gene rearrangements.

[Spatial distribution of fig wasps in syconia of two monoecious Ficus sp].

In addition to pollinator fig wasps, there are several non-pollinating fig wasps associated with monoecious Ficus sp. In order to understand how pollinator fig wasps and non-pollinating fig wasps are distributed across the same syconium, the spatial distribution of fig wasps associated with Ficus altissima and F. benjamina were compared using the pedicle lengths of galls containing each species. The results indicate that in Ficus altissima, the average pedicel length of galls containing Eupristina sp. is longer than that containing E. altissima. Average pedicel length of galls containing Sycobia sp., Micranisa ralianga and Sycoscapter sp. two did not show significant difference. The range of pedicel lengths of galls containing Sycobia sp., M. ralianga or Sycoscapter sp. two is narrower than that of galls containing E. altissima, indicating these non-pollinating fig wasps and pollinator have partially separated spatial niches. In F. benjamina, E. koningsbergeri was distributed in galls from the outer layer to inner layer, while most Walkerella sp. were found in outer layer galls, indicating E. koningsbergeri and Walkerella sp. have partially separated spatial niches.

[Oviposition timing and community structure of Ficus curtipes fig wasps].

Through the behavioral observation of Ficus curtipes fig wasps and the counting of various kinds of flowerets in F. curtipes figs, the oviposition timing and community structure of 12 F. curtipes fig wasp species were studied. Besides the agaonid wasp Eupristina sp., the two non-agaonid wasps Diaziella yangi and Lipothymus sp. could enter into F. curtipes figs and oviposit. The other nine non-agaonid fig wasps ( Walkerella sp., Micranisa sp., Sycophilomorpha sp., Philotrypesis sp., Sycosapter sp., Sycobia sp., Ficomila sp., Ormyrus sp. and Sycophila sp.) oviposited outside the figs. In the fig wasp community, Eupristina sp. was the dominant species, accounting for 62.11% of the total, D. yangi and Lipothymus sp. accounted for 27.19% and 4.71%, respectively, while the other nine non-agaonid fig wasp species only occupied 5.99%. The non-agaonid fig wasps produced their progeny through the reproduction strategies of oviposition timing and diet allocation of female flowerets, so as to sustain the fig-wasp mutualism. The individuals of non-agaonid fig wasp progeny had significant negative correlation with those of agaonid fig wasp progeny, but no correlation with F. curtipes seed production.