Paul Hanson

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.].

Phylogeny and evolution of life-history strategies in the Sycophaginae non-pollinating fig wasps (Hymenoptera, Chalcidoidea)

BackgroundNon-pollinating Sycophaginae (Hymenoptera, Chalcidoidea) form small communities within Urostigma and Sycomorus fig trees. The species show differences in galling habits and exhibit apterous, winged or dimorphic males. The large gall inducers oviposit early in syconium development and lay few eggs; the small gall inducers lay more eggs soon after pollination; the ostiolar gall-inducers enter the syconium to oviposit and the cleptoparasites oviposit in galls induced by other fig wasps. The systematics of the group remains unclear and only one phylogeny based on limited sampling has been published to date. Here we present an expanded phylogeny for sycophagine fig wasps including about 1.5 times the number of described species. We sequenced mitochondrial and nuclear markers (4.2 kb) on 73 species and 145 individuals and conducted maximum likelihood and Bayesian phylogenetic analyses. We then used this phylogeny to reconstruct the evolution of Sycophaginae life-history strategies and test if the presence of winged males and small brood size may be correlated.ResultsThe resulting trees are well resolved and strongly supported. With the exception of Apocrytophagus, which is paraphyletic with respect to Sycophaga, all genera are monophyletic. The Sycophaginae are divided into three clades: (i) Eukoebelea; (ii) Pseudidarnes, Anidarnes and Conidarnes and (iii) Apocryptophagus, Sycophaga and Idarnes. The ancestral states for galling habits and male morphology remain ambiguous and our reconstructions show that the two traits are evolutionary labile.ConclusionsThe three main clades could be considered as tribes and we list some morphological characters that define them. The same biologies re-evolved several times independently, which make Sycophaginae an interesting model to test predictions on what factors will canalize the evolution of a particular biology. The ostiolar gall-inducers are the only monophyletic group. In 15 Myr, they evolved several morphological adaptations to enter the syconia that make them strongly divergent from their sister taxa. Sycophaginae appears to be another example where sexual selection on male mating opportunities favored winged males in species with small broods and wingless males in species with large broods. However, some species are exceptional in that they lay few eggs but exhibit apterous males, which we hypothesize could be due to other selective pressures selecting against the re-appearance of winged morphs.

The Nearctic species of Ormyrus Westwood (Hymenoptera: Chalcidoidea: Ormyridae).

The 16 Nearctic species of Ormyrus are revised; seven new species are described (acylus sp. n., crassus sp. n., reticulatus sp. n., setosus sp. n., tenuis sp. n., turio sp. n., and venustus sp. n.); five new specific synonymies are proposed (labotus Walker = quercipilulae Fitch, quercus Ashmead, brunneipes Provancher, ventricosus Ashmead, and minutus Ashmead). Relationships of the genus are discussed as well as generic limits, and one genus is newly synonymized with Ormyrus (Avrasyamyrus Doganlar). A key to the Nearctic species is presented, and descriptions or re-descriptions are offered for all species, as well as information on hosts and biology. Geographic distributions of closely associated members of three trophic levels are compared: oak, cynipid, and Ormyrus species.

Population trends and damage patterns of Hypsipyla grandella (Lepidoptera: Pyralidae) in a mahogany stand, in Turrialba, Costa Rica

Abstract  1 Population trends of Hypsipyla grandella and their relationship with abiotic (humidity, precipitation and temperature) and biotic factors (availability of mahogany shoots and natural mortality agents), as well as damage patterns, were studied for 16 months in Turrialba, Costa Rica.

A phytophagous braconid, Allorhogas conostegia sp. nov. (Hymenoptera: Braconidae), in the fruits of Conostegia xalapensis (Bonpl.) D. Don (Melastomataceae)

Before 1989 all braconid wasps were thought to be parasitoids, but in that year the first phytophagous species was reported. Subsequently, a few other examples of phytophagy have been discovered, most of which are species of Allorhogas in the subfamily Doryctinae. Until now, all demonstrated examples of phytophagy in this genus have been as gall inducers in the fruits of Fabaceae. Here we describe a new species from Costa Rica, Allorhogas conostegia Marsh and Shaw, and provide evidence that it forms galls in the fruits of Conostegia xalapensis (Melastomataceae). We also provide information on the phenology of the plant and of the galls and the effects of the galls on the host plant, and we discuss the potential species richness of Allorhogas in the Neotropics.

Systematics and evolution of gall formation in the plant‐associated genera of the wasp subfamily Doryctinae (Hymenoptera: Braconidae)

Gall formation is a specialised form of phytophagy that consists of abnormal growth of host plant tissue induced by other organisms, principally insects and mites. In the mainly parasitoid wasp subfamily Doryctinae, gall association, represented by gall inducers, inquilines and their parasitoids, is known for species of seven genera. Previous molecular studies recovered few species of six of these genera as monophyletic despite their disparate morphologies. Here, we reconstructed the evolutionary relationships among 47 species belonging to six gall‐associated doryctine genera based on two mitochondrial and two nuclear gene markers. Most of the Bayesian analyses, performed with different levels of incomplete taxa and characters, supported the monophyly of gall‐associated doryctines, with Heterospilus (Heterospilini) as sister group. Percnobracon Kieffer and Jörgensen and Monitoriella Hedqvist were consistently recovered as monophyletic, and the validity of the monotypic Mononeuron was confirmed with respect to Allorhogas Gahan. A nonmonophyletic Allorhogas was recovered, although without significant support. The relationships obtained and the gathered morphological and biological information led us to erect three new genera originally assigned to Psenobolus: Ficobolus gen.n. (F. paniaguai sp.n. and F. jaliscoi sp.n.), Plesiopsenobolus gen.n. (Pl. mesoamericanus sp.n., Pl. plesiomorphus van Achterberg and Marsh comb.n., and Pl. tico sp.n.), and Sabinita gen.n. (S. mexicana sp.n.). The origin of the gall‐associated doryctine clade was estimated to have occurred during the middle Miocene to early Oligocene, 16.33–30.55 Ma. Our results support the origin of true gall induction in the Doryctinae from parasitoidism of other gall‐forming insects. Moreover, adaptations to attack different gall‐forming taxa on various unrelated plant families probably triggered species diversification in the main Allorhogas clade and may also have promoted the independent origin of gall formation on at least three plant groups. Species diversification in the remaining doryctine taxa was probably a result of host shifts within a particular plant taxon and shifts to different plant organs.

Hopper (Homoptera: Auchenorrhyncha) diversity in shaded coffee systems of Turrialba, Costa Rica

Diversity of hopper species (suborder Auchenorryncha) in coffee (Coffea arabica) plantations with no shade (C) was compared with the diversity in plantations with shade of either poró (Erythrina poeppigiana) (CP) or poró plus laurel (Cordia alliodora) (CPL) in Turrialba, Costa Rica. Species-abundance and rarefaction curves were plotted for each system, and indices of diversity (Shannon-Wiener), dominance (Simpson), species evenness, and similarity (Jaccard) were calculated. The majority of hopper species and individuals belonged to the Cicadellidae family. A particular species dominated in each system: Graphocephala sp. (C), Fusigonalia lativittata (CP) and Hebralebra nicaraguensis (CPL). The richness and diversity of hopper species were highest in the CP system, followed by the CPL and C systems. Species similarity was closest between the CP and CPL systems, but varied considerably according to plant component and geographic location of each plot. Even though hoppers have not been reported as coffee pests in Mesoamerica, some of them cause serious problems elsewhere.

Interactive effects of habitat fragmentation and microclimate on trap-nesting Hymenoptera and their trophic interactions in small secondary rainforest remnants

The combined effects of habitat fragmentation and climate change on biodiversity and biotic interactions are poorly understood. In the context of ongoing deforestation and agricultural intensification in the tropics secondary rainforest fragments might contribute to biodiversity conservation and mitigation of climate warming. This study investigated the interactive effects of habitat fragmentation and microclimate on the abundance and biotic interactions of trap-nesting bees and wasps in secondary forest fragments in the northwestern lowlands of Costa Rica. Fragment size did not affect hymenopteran abundance, parasitism and mortality rates, but all variables differed between edge and interior locations in the forest fragments. Interactive effects between size and location indicate higher mortality rates at interior locations in larger fragments. Microclimatic differences at edge and interior locations led to significant effects on all tested response variables. Abundance at interior locations was significantly higher with increasing temperatures. Mortality rates at interior location increased at lower mean temperatures, whereas higher temperatures at edges marginally increased mortality rates. Our results indicate that edge effects, mediated by altered microclimatic conditions, significantly change biotic interactions of trap-nesting hymenopterans in small secondary fragments.

A new genus of oak gallwasps, Zapatella Pujade-Villar & Melika, gen. n., with a description of two new species from the Neotropics (Hymenoptera, Cynipidae, Cynipini).

Abstract A new genus of cynipid oak gallwasp, Zapatella Pujade-Villar & Melika, gen. n. (Hymenoptera: Cynipidae: Cynipini), with two new species, Zapatella grahami Pujade-Villar & Melika, sp. n. and Zapatella nievesaldreyi Melika & Pujade-Villar, sp. n., is described from the Neotropics. Zapatella grahami,known only from the sexual generation,induces galls in acorns of Quercus costaricensis and is currently known only from Costa Rica. Zapatella nievesaldreyi, known only from the asexual generation, induces inconspicuous galls in twigs of Quercus humboldtii, and is known only from Colombia. Diagnostic characters for both new species are given in detail. Five Nearctic species are transferred from Callirhytis to Zapatella: Zapatella cryptica (Weld), comb. n., Zapatella herberti (Weld), comb. n., Zapatella oblata (Weld), comb. n., Zapatella quercusmedullae (Ashmead), comb. n., Zapatella quercusphellos (Osten Sacken), comb. n. (= Zapatella quercussimilis (Bassett), syn. n.). A key based on adults for the species belonging to Zapatella is also given. Generic limits and morphological characteristics of Zapatella and closely related genera are discussed.

Interactions among three trophic levels and diversity of parasitoids: a case of top-down processes in Mexican tropical dry forest.

Abstract The objective of this study was to analyze the relationship between plant hosts, galling insects, and their parasitoids in a tropical dry forest at Chamela-Cuixmala Biosphere Reserve in western Mexico. In 120 transects of 30 by 5 m (60 in deciduous forest and 60 in riparian habitats), 29 galling insects species were found and represented in the following order: Diptera (Cecidomyiidae, which induced the greatest abundance of galls with 22 species; 76%), Homoptera (Psylloidea, 6.9%; Psyllidae, 6.9%; Triozidae, 3.4%), Hymenoptera (Tanaostigmatidae, 3.4%; which were rare), and one unidentified morphospecies (3.4%). In all cases, there was a great specificity between galling insect species and their host plant species; one galling insect species was associated with one specific plant species. In contrast, there was no specificity between parasitoid species and their host galling insect species. Only 11 species of parasitoids were associated with 29 galling insect species represented in the following families: Torymidae (18.2%), Eurytomidae (18.2%), Eulophidae (18.2%), Eupelmidae (9.1%), Pteromalidae (9.1%), family Braconidae (9.1%), Platygastridae (9.1%), and one unidentified (9.1%). Most parasitoid species parasitized several gall species (Torymus sp.: 51.1%, Eurytoma sp.: 49.7%, Torymoides sp.: 46.9%). Therefore, the effects of variation in plant defenses do not extend to the third trophic level, because a few species of parasitoids can determine the community structure and composition of galling insect species in tropical plants, and instead, top-down processes seem to be regulating trophic interactions of galling insect species in tropical gall communities.