Euphorine phylogeny: the evolution of diversity in host-utilization by parasitoid wasps (Hymenoptera: Braconidae)

ABSTRACT.

• 1 New data on the phylogeny of the braconid subfamily Euphorinae supports the hypothesis that parasitism of adult insects by Euphorinae originated during parasitism of Chrysomelidae, a group whose larvae are ecologically coincident with adults.
• 2 Evolution of the habit of attacking the adult stage opened a new adaptive zone; subsequently the Euphorinae have diversified on to a phylogenetically greater variety of hosts than any other braconid subfamily.
• 3 Parasitism of eumastacid grasshoppers evolved from beetle parasitism in the tribe Perilitini.
• 4 The tribe Euphorini shows the greatest diversity of hosts utilized. Most attack Heteroptera; however, Chrysopopthorus diversified on to adult Chrysopidae, Euphoriella on to Psocoptera, and Cryptoxilos on to Scolytidae.
• 5 Parasitism of bark beetles (Scolytidae) has evolved independently in three genera: Cosmophorus, Cryptoxilos and Ropalophorus. This is the most specialized form of beetle parasitism by euphorines, since it involves direct parasitism of concealed hosts.
• 6 Parasitism of adult hymenopterans by the tribe Syntretini may be related to attacking hosts while they are foraging at flowers.
• 7 The pattern of diversification in the Euphorinae indicates several adaptive radiations within host orders, as well as a history of major host-shifts between phylogenetically distantly-related host groups: Coleoptera to Orthoptera; Coleoptera to Hymenoptera; Coleoptera to Heteroptera; Heteroptera to Neuroptera, Psocoptera, and back to Coleoptera. Both the‘host taxonomy’and‘host habitat’hypotheses of host-shifting are supported. Host-shifts have involved hosts occurring in the same micro-habitat and usually having similar feeding habits. This is consistent with current theory of host-location by means of host-produced kairomones and visual cues.

     

基于28S rRNA基因D2序列的优茧蜂亚科分子系统发育（膜翅目：茧蜂科）

The D2 variable region of 28S ribosomal RNA was sequenced from ethanol specimens or obtained from the literature to provide the first phylogenetie reconstruction of the subfamily Euphorinae (Hymenoptera;Braconidae). Phylogenetic relationships were established by comparing the results using two different methods (distance-based neighbor-joining, NJ; and maximum parsimony, MP) and three different outgroups. The monophyly of the Euphorinae is well supported by all trees generated from molecular data. All phylogenetic reconstructions yielded trees with very similar topologies that only partially resolved the morphologically defined tribes and the relationships within the subfamily. We found no evidence for the monophyletic natures of the tribes Euphorinl, Dinocampini,Perilitini, Syntretini, Comsophorini and Centisitini, but we did find some evidence for the tribes Meteorini and Microctonini. The monophyletic nature of the tribe Meteodnl was well-supported in all trees. We also found the clade containing the LecythodeUa,Microctonus, Orionis and Streblocera to be a monophyletic group, which corresponded to the tribe Microtonini, with Orionis transferred from the tribe Eupholini into Microtonini.Among the genera of Euphorini our results showed strong support for a paraphyletic nature of this group, which can be roughly divided into two clades, one consisting of Aridelus Wesmaelia, the other of Leiophron Peristenus, suggesting both of which may be given tribal rank. The placement of the genus Chrysopophorus is largely uncertain. Two clades,Dinocampus Perilitus and Cosmophorus Rhopalophorus, were constantly resolved in our analyses, with 42-96 and 97-100 bootstrap value support, respectively, suggesting that both of them form monophyletic groups. For members of the Centistini, Pygostolus may be removed and included in Microctonini or other relative tribe.     

基于28S rDNA D2基因片段与形态特征的优茧蜂亚科系统发育研究

本研究选取优茧蜂亚科Euphorinae(膜翅目Hymenoptera:茧蜂科Braconidae)的8族19属23种作为内群,茧蜂其它6个亚科的8属8种作外群,首次结合同源核糖体28S rDNA D2基因序列片段和41个形态学特征对该亚科进行了系统发育学研究。利用"圆口类"的内茧蜂亚科Rogadinae、茧蜂亚科Braconinae、矛茧蜂亚科Doryctinae的3个亚科为根,以PAUP*4.0和MrBayes3.0B4软件分别应用最大简约法(MP)和贝叶斯法对优茧蜂亚科的分子数据和分子数据与非分子数据的结合体进行了分析;并以PAUP*4.0对优茧蜂亚科的28S rDNA D2基因序列的片段的碱基组成与碱基替代情况进行了分析。结果表明:优茧蜂亚科的28S rDNA D2基因序列片段的GC%含量在40.00%~49.25%之间变动,而对于碱基替代情况来讲,优茧蜂亚科各个成员间序列变异位点上颠换(transversion)大于转换(transition);不同的分析和算法所产生的系统发育树都表明目前根据形态定义出的优茧蜂亚科Euphorinae不是一个单系群,而是一个与蚁茧蜂亚科Neoneurinae和高腹茧蜂亚科Cenocoelinae混杂在一起的并系群;在优茧蜂亚科内部,悬茧蜂族Meterorini和食甲茧蜂族Microctonini(排除猎户茧蜂属Orionis)为单系群,而宽鞘茧蜂族Centistini、大颚茧蜂族Cosmophorini、优茧蜂族Euphorini、瓢虫茧蜂族Dinocampini为并系群;悬茧蜂族Meterorini在优茧蜂亚科Euphorinae内位于基部位置的观点得到部分的支持,同时食甲茧蜂族Microctonini被判定为相对进化的类群。此外对于优茧蜂亚科内各属之间的相互亲缘关系,不同算法所得到的系统发育属的结果不完全一致,这表明优茧蜂亚科内(属及族)的系统发育关系还有待于进一步研究。     

部分具翅昆虫后胸足基骨片的分化与系统发育

从12目具翅昆虫中选出16个代表种,对其后足基骨片的形态特征在不同类群中的衍变进行分析比较,据此构建反映下列初步进化关系的系统树:[Ephemeroptera+(Odonata+Neoptera)]+[Plecoptera+(Megaloptera+Neuroptera+(Orthoptera+(Hemiptera+(...     

Molecular phylogenetics of Braconidae (Hymenoptera: Ichneumonoidea), based on multiple nuclear genes,and implications for classification

This study examined subfamilial relationships within Braconidae, using 4 kb of sequence data for 139 taxa. Genetic sampling included previously used markers for phylogenetic studies of Braconidae (28S and 18S rDNA) as well as new nuclear protein‐coding genes (CAD and ACC). Maximum likelihood and Bayesian inference of the concatenated dataset recovered a robust phylogeny, particularly for early divergences within the family. This study focused primarily on non‐cyclostome subfamilies, but the monophyly of the cyclostome complex was strongly supported. There was evidence supporting an independent clade, termed the aphidioid complex, as sister to the cyclostome complex of subfamilies. Maxfischeria was removed from Helconinae and placed within its own subfamily within the aphidioid complex. Most relationships within the cyclostome complex were poorly supported, probably because of lower taxonomic sampling within this group. Similar to other studies, there was strong support for the alysioid subcomplex containing Gnamptodontinae, Alysiinae, Opiinae and Exothecinae. Cenocoeliinae was recovered as sister to all other subfamilies within the euphoroid complex. Planitorus and Mannokeraia, previously placed in Betylobraconinae and Masoninae, respectively, were moved to the Euphorinae, and may share a close affiliation with Neoneurinae. Neoneurinae and Ecnomiinae were placed as tribes within Euphorinae. A sister relationship between the microgastroid and sigalphoid complexes was also recovered. The helconoid complex included a well‐supported lineage that is parasitic on lepidopteran larvae (macrocentroid subcomplex). Helconini was raised to subfamily status, and was recovered as sister to the macrocentroid subcomplex. Blacinae was demoted to tribal status and placed within the newly circumscribed subfamily Brachistinae, which also contains the tribes Diospilini, Brulleiini and Brachistini, all formerly in Helconinae.     

Phylogeny of Eulophidae (Hymenoptera: Chalcidoidea), with a reclassification of Eulophinae and the recognition that Elasmidae are derived eulophids

Eulophidae is a large and biologically varied family of parasitoid wasps, traditionally split into four subfamilies; Elasmidae is a uniform (single genus) and morphologically distinct family of wasps that are thought to be related to Eulophidae. The D2 region of the 28S rDNA gene (≈ 560 bp) of eighty‐seven species of eulophid, three species of elasmid and sixteen outgroup species in five families was sequenced. Cladograms were constructed, and the results compared with conclusions drawn from morphological studies. The gene was most informative at the level of subfamily and tribe. The monophyly of both Eulophinae and Tetrastichinae is supported; that of Entedoninae and Euderinae is less clear. Results indicate that Eulophinae is a derived group within Eulophidae, rather than an ancestral group as previously thought, and that Elasmus, the sole genus of Elasmidae, belongs within this subfamily. The tribes of Eulophinae are reassessed and only three accepted: Eulophini (including Euplectrini and Elachertini), Elasmini and Cirrospilini LaSalle trib.n. for Bou?ek's Ophelimini with Ophelimus and Australsecodes excluded. Three small Australian tribes, Anselmellini, Ophelimini and Platytetracampini, are removed from Eulophinae and Entedoninae, respectively, but their exact relationships and subfamily status cannot as yet be decided. Another tribe, Keryini, known from a single Australian genus, is excluded from both Eulophinae and Eulophidae.     

Linnaeus,animals and man*

Linnaeus is often undervalued as a zoologist. His importance lies not only in the introduction of binomial nomenclature and his Systema Naturae. As a systematist he divided the insects into the groups, Coleoptera, Hemiptera, Lepidoptera, Neuroptera, Hymenoptera, Diptera and Aptera. His programme, as expressed in his Methodus in Systema Naturae (1st ed.) is astounding in its biological manysidedness. He was before his time in many respects: he wrote and lectured upon bird migration, biological control of insects with their parasites or predators, protective mimicry, the struggle by all organisms for survival, contagious diseases as well as fermentation due to small living particles. He was the first to call attention to the close relationship between man and the anthropoid apes.     

Phylogenomics of the lepidopteran endoparasitoid wasp subfamily Rogadinae (Hymenoptera: Braconidae) and related subfamilies

Rogadinae are a cosmopolitan, species‐rich braconid wasp subfamily whose species are endoparasitoids that attack larvae of a number of lepidopteran families. Members of this subfamily are characterized by pupating within the mummified host larval skin. The subfamily contains six tribes whose relationships have only been partially clarified: Aleiodini, Betylobraconini, Clinocentrini, Rogadini, Stiropiini and Yeliconini. The limits and composition of the closely related subfamilies to the Rogadinae, Hormiinae and Lysiterminae, also remain unclear. Here, we generated ultraconserved element data to reconstruct an almost fully resolved phylogeny for the members of Rogadinae and related subfamilies. Based on our best estimate of phylogeny, we confirm the monophyly of Rogadinae including Betylobraconini, synonymize Xenolobus Fahringer and Bequartia Cameron within the species‐rich genus Aleiodes Wesmael ( syn.n. ) based on DNA, and synonymize Promesocentrus van Achterberg with Pilichremylus Belokobylskij ( syn.n. ) based on morphology. We also consistently recovered Hormiinae and Lysiterminae as not reciprocally monophyletic, and thus propose to unite their members under Hormiinae. The ancestral host preference for Rogadinae was probably attacking concealed lepidopteran larvae, with the occurrence of at least two main subsequent transitions to attack both concealed and exposed hosts, one within Rogadini and a second within Aleiodini. We highlight the importance of natural history collections as a source for conducting genomic‐based studies using techniques that allow to obtain a substantial amount of data from considerably old preserved insect specimens.     

Seasonal pattern of insect abundance in the Brazilian cerrado

Abstract In Brazil, a severe dry season lasting for approximately 5 months and frequent fires make life difficult for cerrado insects. In certain aspects, the cerrado can be considered to be an understudied ecosystem; even basic information such as knowledge about the annual peak in abundance of different insect orders is unknown. Insect abundance patterns have only been investigated for a few groups in the cerrado region. Thus, our study concerns the temporal distribution of insect abundance in the savanna‐like vegetation of the central Brazilian cerrado (sensu stricto) in Distrito Federal. The region has a well‐defined, long dry season between May and September. The insects were sampled by window, malaise tent and pitfall traps within 1 year. We used a multiple linear regression to analyse the relationship between abundance of insects of each order and climate variables. A total of 50 127 individuals from 15 orders was collected. The orders were Coleoptera (26%), Hymenoptera (23%), Diptera (20.5%), Isoptera (20%), Homoptera (4%), Lepidoptera (4%), Orthoptera (1.5%) and Hemiptera (1%). The abundance of Diptera, Homoptera, Lepidoptera and Orthoptera was randomly distributed over time, Isoptera peaked in the first half of the wet season, Coleoptera and Hemiptera in the second half of the wet season and Hymenoptera in each season. A significant correlation was found only between Coleoptera and delayed climatic variables. There were no obvious trends that might help explain the abundance patterns observed. The study provides baseline information about phenological patterns of insect abundance and permits evaluation of this group as a resource for various food chains and different trophic levels.     

Wood anatomy of the subfamily Crotonoideae (Euphorbiaceae s.s.) from India: systematic implications with special reference to the taxonomic delimitation of Givotia and Vernicia

The wood anatomy of 15 representative species belonging to 12 genera of nine tribes of the subfamily Crotonoideae (Euphorbiaceae) are comprehensively described with focus on systematic implications. In addition, ecological and evolutionary aspects are evaluated. An identification key to the species based on wood anatomical features is presented. The wood microstructure of the tribes was found to be considerably heterogeneous reflecting an unnatural classification of the subfamily. However, the results confirm the generic relationship within subtribe Aleuritinae and tribe Ricinodendreae. Vernicia and Givotia may be recognized based on wood anatomical and morphological characters. The tribes Micrandreae and Adenoclineae have considerable similarity in wood anatomy. The wood structure of the monogeneric tribes Trigonostemoneae and Geloneae idicate a close relationship with the tribe Crotoneae.     

Long-Term Storage of Infective Microsporidian Spores in Liquid Nitrogen

Thirty-one species of microsporidia, isolated from insects and stored in liquid nitrogen for up to 25 yr, were infectious when removed from liquid nitrogen. The natural hosts of all of these microsporidia were terrestrial insects, representing six different insect orders: Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, and Orthoptera. All microsporidia from terrestrial insects that were tested survived storage in liquid nitrogen, while Nosema algerae , a microsporidium from aquatic mosquito hosts did not survive freezing in liquid nitrogen. A Nosema species from the alfalfa weevil, Hypera postica , lost some infectivity in a water storage medium after 25 yr in liquid nitrogen. Liquid nitrogen storage of microsporidian spores in 50% and 100% glycerol media reduced loss of infectivity and is recommended for extended storage of microsporidia from terrestrial insect hosts.     

New and little known planthoppers of the subfamily Ommatidiotinae (Homoptera,Fulgoroidea, Caliscelidae) from Madagascar and South Asia

Cano merinus gen. et sp. n., belonging to the tribe Augilini Baker, is described from Madagascar. Tubilustrium typicum Distant, 1916 is transferred from the tribe Ommatidiotini Fieber to the tribe Augilini. Lasonia kirkaldyi Melichar, 1903 is transferred from the family Issidae to the family Caliscelidae, tribe Adenissini Dlabola. A key to the tribes of the subfamily Ommatidiotinae is provided.     

锯凤蝶类和绢蝶类(鳞翅目,凤蝶科)分类地位及系谱关系初探

锯凤蝶族Zerynthiini的分类地位一直受到国内外学者的关注.本文对锯凤蝶族Zerynthiini、绢蝶族Parnassiini及凤蝶亚科Papilioninae中相关族的幼虫形态、翅脉、翅面斑纹、鳞片、雌性交配栓、雄性外生殖器、地理分布与历史变迁,进行了比较研究,对这些类群的亲缘关系进行了初步探讨.结果表明:锯凤蝶族可能是由绢蝶亚科某一古老或已灭绝的族中演化而来,应作为绢蝶亚科下的一个族,不应作为亚科对待;锯凤蝶族和绢蝶族同属绢蝶亚科,绢蝶亚科和凤蝶亚科同属凤蝶科.     

Trichome anatomy of the Saxifragaceae S. l.from the southern hemisphere

Trichome anatomy was examined by light and scanning electron microscopy in 25 genera of Engler's Saxifragaceae from the southern hemisphere. Four principal categories of trichome were recognized: (1) multiseriate with a glandular head; (2) uniseriate with a glandular head; (3) uniseriate, eglandular; (4) unicellular, eglandular. The shape of eglandular hairs ranges from erect to sickle-shaped to T-shaped. The main taxonomic conclusions are as follows: (a) Vahlia should be excluded from tribe Saxifrageae and a possible relationship with Montinia investigated; (b) Francoa and Tetilta (tribe Francoeae) are closely related, although the relationship of the tribe to its parent subfamily, Saxifragoideae, is unclear; (c) Eremosyne is probably allied to the Escallonioideae; (d) subfamily Brexioideae is heterogeneous in trichome anatomy, but the relationships of its constituent genera remain problematic; (e) subfamily Escallonioideae is heterogeneous in trichome anatomy, although similarities between and within the constituent tribes do exist. Thus Cuttsia and Abrophyllum form a natural group (tribe Cuttsieae), to which Carpodetus (tribe Argophylleae) may also be related; similarity in trichome anatomy between Argophyttum and Corokia (tribe Argophylleae) is substantiated by an extensive survey of all the species, and the data tentatively suggest a possible hydrangeoid affinity for these two genera.Forgesia (tribe Forgesieae) is shown to possess the same kind of hairs in the flowers as Quintinia (tribe Escallonieae), and Choristylis (tribe Forgesieae) is shown to be remarkably similar to Escallonia, prompting a suggestion that the two tribes be merged. Trichome data support the inclusion of Anopterus and Polyosma in their own tribes, although their wider affinities remain unclear. Doubts about the inclusion of the glabrous Tribeles in Escallonioideae are expressed. Our material of the following additional genera Lepuropetalon, Tetracarpaea and Brexia was glabrous and little comment could be made about them.     

Recognition of heterospecific parasitism: Competition between Aphidiid (Aphidius ervi) and Aphelinid (Aphelinus asychis) parasitoids of Aphids (Hymenoptera: Aphidiidae; Aphelinidae)

The solitary parasitoids Aphidius erviHaliday (Hymenoptera: Aphidiidae) and Aphelinus asychisWalker (Hymenoptera: Aphelinidae) attacked but generally did not oviposit in pea aphids parasitized by the other species. Wasps selectively oviposited in unparasitized hosts when given a choice. Host discrimination depended on the recognition of internal cues. Females of A. asychiseither could not recognize or ignored A. ervi'sexternal host marking pheromone. Under most conditions, A. ervisurvived in superparasitized hosts, killing competing A. asychislarvae by physical attack and possibly physiological suppression. The outcome of larval competition was not affected by oviposition sequence or age difference between larvae; A. asychissurvived only when it had substantially completed larval development before the host was superparasitized by A. ervi.It is suggested that competition for host resources incurs a cost, for the winner in terms of reduced size or increased development time and for the loser in terms of lost progeny and searching time. Consequently, heterospecific host discrimination can be functional. Internal, and probably general, cues enable wasps to recognize and avoid oviposition in hosts already parasitized by an unrelated species.     

Diversity and abundance of insect visitors to flowers of trees and shrubs in a South African savannah

This study presents the results of a landscape‐scale survey for insect floral visitors in the Skukuza Ranger District, Kruger National Park, South Africa. Floral visitors were sampled from flowering trees and shrubs along linear transects spanning the entire district. Six plant species were sampled in the late dry season (Acacia grandicornuta Gerstner, A. nigrescens Oliver, Cassia abbreviata Oliver, Combretum hereroense Schinz, Combretum zeyheri Sonder, Euclea divonorum Hiern), and eleven plant species were sampled during the rainy season (Acacia exuvialis Verdcourt, A. grandicornuta Gerstner, A. nilotica (L.) Willdenow, A. tortilis (Forsskal) Hayne, Dichrostachys cinerea Miquel, Flueggea virosa (Roxburgh) Baillon, Grewia bicolor Jussieu, G. flava De Candolle, G. flavescens Jussieu, G. monticola Sonder, and Peltophorum africanum Sonder). Coleoptera, Hymenoptera and Lepidoptera comprised the majority of floral visitors, while species of Blattodea, Diptera, Hemiptera and Neuroptera also occurred on flowers. Known or likely pollinators include bees (Hymenoptera: Apidae, Halictidae and Megachilidae) and scarab beetles (Coleoptera: Scarabaeidae). These plant species appear to have generalist pollination systems, with the exception of species of Grewia L., which appear to be pollinated primarily by bees. A provisional plant–pollinator food web is presented for the eleven species of trees and shrubs which flower during the rainy season.     

Competitive interactions between parasitoid larvae and the evolution of gregarious development

We report experiments using two closely related species of alysiine braconids directed at understanding how gregarious development evolved in one subfamily of parasitoid wasps. Theoretical models predict that once siblicide between parasitoid wasps has evolved, it can only be lost under stringent conditions, making the transition from solitary to gregarious development exiguous. Phylogenetic studies indicate, however, that gregariousness has independently arisen on numerous occasions. New theoretical models have demonstrated that if gregarious development involves reductions in larval mobility, rather than a lack of fighting ability (as in the older models), the evolution of gregariousness is much more likely. We tested the predictions of the older tolerance models (gregariousness based on non-fighting larval phenotypes) and the reduced mobility models (gregariousness based on non-searching larval phenotypes) by observing larval movement and the outcome of interspecific competition between Aphaereta genevensis (solitary) and A. pallipes (gregarious) under multiparasitism. Differences in larval mobility matched the prediction of the reduced mobility model of gregarious development, with the solitary A. genevensis having larvae that are much more mobile. The proportion of hosts producing the solitary species significantly declined after subsequent exposure to females of the gregarious species. This contradicts the prediction of the older models (fighting vs non-fighting phenotypes), under which any competitive interactions between solitary and gregarious larvae will result in a highly asymmetrical outcome, as the solitary species should be competitively superior. The observed outcome of interspecific competition offers evidence, with respect to this subfamily, in favour of the new models (searching vs non-searching phenotypes).     

Flowers for better pest control? The effects of apple orchard ground cover management on green apple aphids (Aphis spp.) (Hemiptera: Aphididae), their predators and the canopy insect community

Effects of habitat diversification through ground cover management on green apple aphids (Aphis spp.) (Hemiptera: Aphididae), woolly apple aphid (Eriosoma lanigerum [Haussmann]) (Hemiptera: Aphididae), their insect natural enemies and the most abundant canopy insects (in the Neuroptera, Fulgoromorpha, Cicadomorpha, Heteroptera, Coleoptera and Formicidae) were studied in an apple orchard over 6 years. The composition and diversity of the main functional groups of canopy insects was also compared. Habitat diversification was achieved by changing ground cover conditions within the orchard. In the treatment termed FLOWER, annual and/or perennial flowering plants were sown in the alleys of an apple orchard. Other ground cover treatments were weed-free bare ground (termed BAREgr) and orchard plots with alleys of mowed grass (termed GRASS), which served as control treatments. We found no evidence that habitat diversification enhanced the biological control of green apple aphids compared to the control treatments. However, the greater plant cover in FLOWER resulted in increased woolly apple aphid infestations compared to BAREgr or GRASS. The abundance of various beneficial or neutral canopy insects – Chrysoperla carnea sensu lato (Neuroptera, Chrysopidae) adults, leafhoppers and treehoppers, planthoppers, herbivorous (non-apple feeding) beetles, dipterans and parasitoid wasps – also increased in FLOWER as compared to BAREgr, with GRASS being intermediate between the other treatments. Significantly greater species richness and diversity was found in FLOWER than in BAREgr for most of the functional groups sampled, although the number of predacious insect species was similar among treatments. The composition of the studied functional groups showed high similarity in FLOWER and GRASS, but these treatments were different from BAREgr. Effects of groundcover management on the dominant insect species are discussed.