Allopatric distribution and diversification without niche shift in a bryophyte-feeding basal moth lineage (Lepidoptera: Micropterigidae)

The Lepidoptera represent one of the most successful radiations of plant-feeding insects, which predominantly took place within angiosperms beginning in the Cretaceous period. Angiosperm colonization is thought to underlie the evolutionary success of the Lepidoptera because angiosperms provide an enormous range of niches for ecological speciation to take place. By contrast, the basal lepidopteran lineage, Micropterigidae, remained unassociated with angiosperms since Jurassic times but nevertheless achieved a modest diversity in the Japanese Archipelago. We explored the causes and processes of diversification of the Japanese micropterigid moths by performing molecular phylogenetic analysis and extensive ecological surveying. Phylogenetic analysis recovered a monophyletic group of approximately 25 East Asian endemic species that feed exclusively on the liverwort Conocephalum conicum, suggesting that niche shifts hardly played a role in their diversification. Consistent with the low flying ability of micropterigid moths, the distributions of the Conocephalum specialists are each localized and allopatric, indicating that speciation by geographical isolation has been the major process shaping the diversity of Japanese Micropterigidae. To our knowledge, this is the largest radiation of herbivorous insects that does not accompany any apparent niche differentiation. We suggest that the significance of non-ecological speciation during the diversification of the Lepidoptera is commonly underestimated.     

Factors influencing diversification in angiosperms: at the crossroads of intrinsic and extrinsic traits

Recent studies indicate that both key innovations and available area influence species richness in angiosperms. Available area has been observed to have the greatest effect, however, and appears to alter the "carrying capacity" of a lineage rather than alter diversification rates. Here, we review and weigh the evidence of predictors of angiosperm diversification and further dissect how area can place ecological limits on diversification of angiosperms, specifically addressing the following: (1) theoretical mechanisms by which particular intrinsic and extrinsic traits may affect diversification in angiosperm families; (2) evidence that the amount of available area determines the ecological limits on lineages; and (3) geographical distribution of diversification hotspots in angiosperms, concentrating on the effects of zygomorphy, noncontiguous area, and latitude. While we found that dispersal to numerous noncontiguous areas is most important in spurring diversification, diversification of tropical and zygomorphic families appears to be elevated by the generation of more species per given area.     

Timing and Patterns in the Taxonomic Diversification of Lepidoptera (Butterflies and Moths)

The macroevolutionary history of the megadiverse insect order Lepidoptera remains little-known, yet coevolutionary dynamics with their angiospermous host plants are thought to have influenced their diversification significantly. We estimate the divergence times of all higher-level lineages of Lepidoptera, including most extant families. We find that the diversification of major lineages in Lepidoptera are approximately equal in age to the crown group of angiosperms and that there appear to have been three significant increases in diversification rates among Lepidoptera over evolutionary time: 1) at the origin of the crown group of Ditrysia about 150 million years ago (mya), 2) at the origin of the stem group of Apoditrysia about 120 mya and finally 3) a spectacular increase at the origin of the stem group of the quadrifid noctuoids about 70 mya. In addition, there appears to be a significant increase in diversification rate in multiple lineages around 90 mya, which is concordant with the radiation of angiosperms. Almost all extant families appear to have begun diversifying soon after the Cretaceous/Paleogene event 65.51 mya.     

One fig to bind them all: host conservatism in a fig wasp community unraveled by cospeciation analyses among pollinating and nonpollinating fig wasps

The study of chalcid wasps that live within syconia of fig trees (Moraceae, Ficus ), provides a unique opportunity to investigate the evolution of specialized communities of insects. By conducting cospeciation analyses between figs of section Galoglychia and some of their associated fig wasps, we show that, although host switches and duplication have evidently played a role in the construction of the current associations, the global picture is one of significant cospeciation throughout the evolution of these communities. Contrary to common belief, nonpollinating wasps are at least as constrained as pollinators by their host association in their diversification in this section. By adapting a randomization test in a supertree context, we further confirm that wasp phylogenies are significantly congruent with each other, and build a "wasp community" supertree that retrieves Galoglychia taxonomic subdivisions. Altogether, these results probably reflect wasp host specialization but also, to some extent, they might indicate that niche saturation within the fig prevents recurrent intrahost speciation and host switching. Finally, a comparison of ITS2 sequence divergence of cospeciating pairs of wasps suggests that the diversification of some pollinating and nonpollinating wasps of Galoglychia figs has been synchronous but that pollinating wasps exhibit a higher rate of molecular evolution.     

Bimodal Pollination by Wasps and Beetles in the African Milkweed Xysmalobium undulatum

It has been suggested that flowers of some plants are specialized for pollination by two unrelated species (or functional groups) of pollinators. However, evidence for 'bimodal pollination systems' has been extremely limited. Studies of the milkweed Xysmalobium undulatum in South Africa showed that its flowers are visited by a range of different insects (representing 18 families), but only two groups, represented by the chafer beetle Atrichelaphinis tigrina and pompilid wasps in the genus Hemipepsis , effect pollination. Experiments showed that both these pollinator groups are effective in removing and inserting pollinia. Pollinia are attached to clypeal hairs and mouthparts on the wasps and tarsal hairs and spines on the beetles. Although considerably less abundant than the beetles, Hemipepsis spp. wasps move more quickly among flowers and appeared to be more effective pollinators overall. Experimental hand-pollinations conducted in the field showed that X. undulatum is genetically self-incompatible and thus completely reliant on pollinators for reproduction. We conclude that X. undulatum has a bimodal pollination system, specialized for pollination by Hemipepsis pompilid wasps and the chafer beetle A. tigrina .     

Timing in the evolution of derived floral characters: upper cretaceous (turonian) taxa with tricolpate and tricolpate-derived pollen

Various hypotheses that seek to explain the rich species diversity of angiosperms relative to other seed plants are briefly mentioned or reviewed. Of these, the subset that relates angiosperm diversity in some way to the relationship between angiosperms and insects, particularly anthophilous insects, is here the object of attention. Specifically, I address and reject the possibility that the relationship between angiosperm diversification and insects, particularly those demonstrating a preference for flowers with derived floral characteristics associated with insect pollination, may be ruled out because of asynchronous patterns of diversification in the fossil record. New data on floral structure from the Turonian of the Atlantic Coastal Plain reveal a surprising diversity of floral characters in taxa bearing tricolpate and tricolporate-derived pollen. The characters and taxa that appear in these Turonian sediments suggest that rather specific modes of insect pollination, perhaps involving highly derived insect pollinators, already existed at 90 Ma. Given the observed rate of diversification of angiosperms during that time and the pattern of evolution in insects, including what can be inferred about the history of the Apidae, these new floral data suggest that hypotheses relating angiosperm diversity to highly specific pollinators are still valid in the context of fossil evidence. Even so, consistency with fossil evidence is not necessarily proof of these relationships. In any case, there may well be multiple causes of relatively high angiosperm species diversity and understanding the relative importance of each of these requires neontological as well as paleontological investigations. One promising approach is to work within the context of phylogenetic patterns with more fossil data.     

Angiosperm growth habit,dispersal and diversification reconsidered

Summary Previous studies have sought to elucidate the relationship between dispersal mode (biotic versus abiotic) and the taxonomic diversification of angiosperm families, but with ambiguous results. In this study, we propose the hypothesis that the combination of (1) the large seed size required of plants germinating in closed, light-poor environments and (2) the necessity to move disseminules away from the maternal plant in order to avoid intraspecific competition, predation and pathogens should favour biotically-dispersed relative to abiotically-dispersed woody arborescent angiosperms, resulting in higher diversification of the former. In this paper, we seek patterns of diversification that support this hypothesis. We examine the association between dispersal mode, growth habit and taxonomic richness of monocotyledon and dicotyledon families using (1) contingency table analyses to detect the effect of dispersal mode on the relative abundances and diversification of woody versus herbaceous taxa and (2) non-parametric analyses of variance to detect the statistical effect of dispersal mode on taxonomic diversification (mean number of species per genus, genera per family and species per family) in monocot and dicot families dominated by biotic or abiotic dispersal. We found a clear statistical effect of dispersal mode on diversification. Among families of woody dicots, dispersal by vertebrates is associated with significantly higher levels of species per genus, genera per family and species per family than is abiotic dispersal. The same pattern is observed among woody monocots, but is not significant at the 0.05 level. Among families of herbaceous monocots and dicots, the situation is reversed, with abiotically-dispersed families exhibiting higher levels of diversification than vertebrate-dispersed families. When woody and herbaceous families are pooled, there is no association between dispersal mode and diversification. These data coincide with evidence from the fossil record to suggest vertebrate dispersal has positively contributed to the diversification of woody angiosperms. We suggest that vertebrate dispersal may have promoted the diversity of extant taxa by reducing the probability of extinction over evolutionary time, rather than by elevating speciation rates. Our results suggest vertebrate dispersal has contributed to, but does not explainin toto, the diversity of living angiosperms.     

Molecular evolution of the petal and stamen identity genes, APETALA3 and PISTILLATA, after petal loss in the Piperales

Organ loss is an evolutionary phenomenon commonly observed in all kinds of multicellular organisms. Across the angiosperms, petals have been lost several times over the course of their diversification. We examined the evolution of petal and stamen identity genes in the Piperales, a basal lineage of angiosperms that includes the perianthless (with no petals or sepals) families Piperaceae and Saururaceae as well as the Aristolochiaceae, which exhibit a well-developed perianth. Here, we provide evidence for relaxation of selection on the putative petal and stamen identity genes, homologs of APETALA3 and PISTILLATA, following the loss of petals in the Piperales. Our results are particularly interesting as the B-class genes are not only responsible for the production of petals but are also central to stamen identity, the male reproductive organs that show no modification in these plants. Relaxed purifying selection after the loss of only one of these organs suggests that there has been dissociation of the functional roles of these genes in the Piperales.     

Differences in meristems between monocots and dicots and susceptibility to attack by gall-inducing insects

We used comparative methods that account for the phylogenetic correlations among species to test hypotheses about the community of gall-inducing insects on dicotyledonous and monocotyledonous plants and woody and herbaceous angiosperms in the UK. We found that the species richness of gall-inducing insects on dicots was greater than on monocots and that the odds of a dicot having an associated gall-inducing insect is 42% higher than for a monocot. Woody angiosperms have higher species richness of associated gall-inducing insects than do herbaceous angiosperms. Furthermore, using a Monte Carlo analysis we found that attacks by gall-inducing insects on monocot families were phylogenetically clustered in the order Poales, particularly within the grass family Poaceae. We suggest that the higher risk of attack on dicots and higher species richness of gall-inducing insects on woody angiosperms, which are exclusively dicots, arises because of differences in the abundance or susceptibility of dicot meristems to attack by gall-inducing insects. Architectural and anatomical differences between monocots and dicots that give rise to differences in meristem abundance and anatomy appear to play an important role in determining the occurrence and richness of associated gall-inducing insects on host plants.     

Phylogenetic tree of vascular plants reveals the origins of aquatic angiosperms

Although aquatic plants are discussed as a unified biological group, they are phylogenetically well dispersed across the angiosperms. In this study, we annotated the aquatic taxa on the tree of vascular plants, and extracted the topology of these aquatic lineages to construct the tree of aquatic angiosperms. We also reconstructed the ancestral areas of aquatic families. We found that aquatic angiosperms could be divided into two different categories: the four aquatic orders and the aquatic taxa in terrestrial orders. Aquatic lineages evolved early in the radiation of angiosperms, both in the orders Nymphaeales and Ceratophyllales and among basal monocots (Acorales and Alismatales). These aquatic orders do not have any extant terrestrial relatives. They originated from aquatic habitats during the Early Cretaceous. Asia would have been one of the centers for early diversification of aquatic angiosperms. The aquatic families within terrestrial orders may originate from other areas besides Asia, such as America or Australia. The lineages leading to extant angiosperms diversified early in underexploited freshwater habitats. The four extant aquatic orders were relicts of an early radiation of angiosperm in aquatic environments. Their extinct ancestors might be aquatic early angiosperms.     

Nonstochastic variation of species-level diversification rates within angiosperms

Variations in the origination and extinction rates of species over geological time often are linked with a range of factors, including the evolution of key innovations, changes in ecosystem structure, and environmental factors such as shifts in climate and physical geography. Before hypothesizing causality of a single factor, it is critical to demonstrate that the observed variation in diversification is significantly greater than one would expect due to natural stochasticity in the evolutionary branching process. Here, we use a likelihood-ratio test to compare taxonomic rate heterogeneity to a neutral birth-death model, using data on well-supported sister pairs of taxa and their species richness. We test the likelihood that the distribution of extant species among angiosperm genera and families could be the result of constant diversification rates. Results strongly support the conclusion that there is significantly more heterogeneity in diversity at the species level within angiosperms than would be expected due to stochastic processes. This result is consistent in datasets of genus pairs and family pairs and is not affected significantly by degrading pairs to simulate inaccuracy in the assumption of simultaneous origin of sister taxa. When we parse taxon pairs among higher groups of angiosperms, results indicate that a constant rates model is not rejected by rosid and basal eudicot pairs but is rejected by asterid and eumagnoliid pairs. These results provide strong support for the hypothesis that species-level rates of origination and/or extinction have varied nonrandomly within angiosperms and that the magnitude of heterogeneity varies among major groups within angiosperms.     

Medium molecular weight polar substances of the cuticle as tools in the study of the taxonomy,systematics and chemical ecology of tropical hover wasps (Hymenoptera: Stenogastrinae)

The Stenogastrinae wasps have been proposed as a key group for an understanding of social evolution in insects, but the phylogeny of the group is still under discussion. The use of chemical characters, in particular cuticular hydrocarbons, for insect taxonomy is relatively recent and only a few studies have been conducted on the cuticular polar substances. In this work, we ascertain, by the matrix‐assisted laser desorption ionization‐time of flight mass spectrometry technique, that different species of primitively eusocial hover wasps have different compositions of the epicuticular polar compounds ranging from 900 to 3600 Da. General linear model analysis and discriminant analysis showed that the average spectral profiles of this fraction can be diagnostic for identification of the species. Moreover, for the first time we show population diversification in the medium MW polar cuticular mixtures in insects. In conclusion, the results demonstrate that the chemical characters are consistent with the physical characters and the study support the importance of medium MW polar substances as powerful tools for systematics (chemosystematics) and chemical ecology (fertility signal and population characterization) in a primitively social insect taxon.     

Intra-Population Genetic Variation in the Temporal Pattern of Egg Maturation in a Parasitoid Wasp

Parasitoid wasps are taxonomically and biologically extremely diverse. A conceptual framework has recently been developed for understanding life-history evolution and diversification in these animals, and it has confirmed that each of two linked life-history traits – the mode of larval development and the temporal pattern of egg maturation – acts as an organiser of life-history. The framework has been predicated on the assumption that there exists sufficient genetic variation in the latter trait to allow it to be shaped by natural selection. Focusing on the parasitoid wasp Trichogramma brassicae, our aim was to test the validity of that assumption, using established quantitative genetic methods. We demonstrate the existence of a statistically significant degree of intra-population polygenic variation in the temporal pattern of egg production within the wasp population we studied. Furthermore, our results, together with published data on clinal variation in the egg maturation pattern of another species, suggest that intra-specific evolutionary shifts in the temporal pattern of egg maturation of parasitoid wasps can result from a change in allocation to egg production either before, or very shortly after adult emergence, without there being an accompanying change in lifetime fecundity. As well as opening new avenues of research into the reproductive strategies, behaviour, community organisation and biological control potential of parasitoid wasps, this discovery also has implications for studies of life-history evolution and diversification in insects generally.     

BIRD-INSECT NESTING ASSOCIATIONS IN AUSTRALIA.

Australian records, beginning in 1866, of birds associating with aggressive insects for nesting purposes are assembled. Five species of the genus Gerygone are known to associate with wasps, more or less consistently, in tropical areas, and another species is reported as associating with wasps in the tropics and ants in temperate areas. Such birds deliberately seek the society of the insects, by which they are recognized and tolerated.
If protection is the motive, it would seem to be aimed against reptiles rather than against other birds or mammals. Other possible reasons for the practice ate suggested.
Australian records of insects frequenting birds' nests also are summarized; these include parasites such as the blood-sucking larvae of a fly, together with moth, beetle and fly larvae that serve a beneficial purpose as scavengers, and, in addition, wasps and beetles parasitic on the other insects. On the question of how the insects find the nests at appropriate times, it is suggested that some are guided by odour and others by some undetermined influence.     

Ants Sow the Seeds of Global Diversification in Flowering Plants

Background

The extraordinary diversification of angiosperm plants in the Cretaceous and Tertiary periods has produced an estimated 250,000–300,000 living angiosperm species and has fundamentally altered terrestrial ecosystems. Interactions with animals as pollinators or seed dispersers have long been suspected as drivers of angiosperm diversification, yet empirical examples remain sparse or inconclusive. Seed dispersal by ants (myrmecochory) may drive diversification as it can reduce extinction by providing selective advantages to plants and can increase speciation by enhancing geographical isolation by extremely limited dispersal distances.

Methodology/Principal Findings

Using the most comprehensive sister-group comparison to date, we tested the hypothesis that myrmecochory leads to higher diversification rates in angiosperm plants. As predicted, diversification rates were substantially higher in ant-dispersed plants than in their non-myrmecochorous relatives. Data from 101 angiosperm lineages in 241 genera from all continents except Antarctica revealed that ant-dispersed lineages contained on average more than twice as many species as did their non-myrmecochorous sister groups. Contrasts in species diversity between sister groups demonstrated that diversification rates did not depend on seed dispersal mode in the sister group and were higher in myrmecochorous lineages in most biogeographic regions.

Conclusions/Significance

Myrmecochory, which has evolved independently at least 100 times in angiosperms and is estimated to be present in at least 77 families and 11 000 species, is a key evolutionary innovation and a globally important driver of plant diversity. Myrmecochory provides the best example to date for a consistent effect of any mutualism on large-scale diversification.     

Pollinators of tropical dioecious angiosperms

Dioecy is frequent in tropical forests. It has been suggested that small, unspecialized pollinators are among the factors responsible for gender separation in this habitat. The underlying assumption is that poor fliers and/or communal foragers frequently effect selfing which in turn, given sufficiently severe inbreeding depression, should favor the establishment of dioecy. At least 10% of the genera of the angiosperms includes dioecious species; in tropical flowering plants, however, pollinators are reliably known only in a few species. Whereas temperate dioecious species commonly are wind- or water-pollinated, anemophily is less important in tropical forests, but occurs in at least 30 dioecious genera. Our survey of tropical dioecious zoophilous species in 29 genera (in 21 families) for which detailed pollination information is available shows that these species have specialized flowers adapted to specific pollinators rather than generalized flowers suitable for diverse insects. Known pollinators include solitary and eusocial bees, beetles, moths, flies, wasps (including fig wasps), and rarely bats and birds, and cover a wide range in animal size and locomotive capabilities. Floral rewards comprise pollen, nectar, stylar mucilage, nutritious tissues, brood-places, and resins. About a third of the species offer no reward in the female morph, pollination by deceit apparently being common. Our data thus do not support the hypothesis that there is a broad correlation between a dioecious breeding system and unspecialized pollination, although such a correlation may be found in certain taxa. Specialized plant-pollinator relationships seem as critical in dioecious plants in tropical forests, where individuals often grow far apart, as they are in tropical plants with other breeding systems.     

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.     

The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal-arthropod symbioses

Paleoophiocordyceps coccophagus, a fungal parasite of a scale insect from the Early Cretaceous (Upper Albian), is reported and described here. This fossil not only provides the oldest fossil evidence of animal parasitism by fungi but also contains morphological features similar to asexual states of Hirsutella and Hymenostilbe of the extant genus Ophiocordyceps (Ophiocordycipitaceae, Hypocreales, Sordariomycetes, Pezizomycotina, Ascomycota). Because species of Hypocreales collectively exhibit a broad range of nutritional modes and symbioses involving plants, animals and other fungi, we conducted ancestral host reconstruction coupled with phylogenetic dating analyses calibrated with P.coccophagus. These results support a plant-based ancestral nutritional mode for Hypocreales, which then diversified ecologically through a dynamic process of intra- and interkingdom host shifts involving fungal, higher plant and animal hosts. This is especially evident in the families Cordycipitaceae, Clavicipitaceae and Ophiocordycipitaceae, which are characterized by a high occurrence of insect pathogens. The ancestral ecologies of Clavicipitaceae and Ophiocordycipitaceae are inferred to be animal pathogens, a trait inherited from a common ancestor, whereas the ancestral host affiliation of Cordycipitaceae was not resolved. Phylogenetic dating supports both a Jurassic origin of fungal-animal symbioses within Hypocreales and parallel diversification of all three insect pathogenic families during the Cretaceous, concurrent with the diversification of insects and angiosperms.     

Multigene analyses identify the three earliest lineages of extant flowering plants

Flowering plants (angiosperms) are by far the largest, most diverse, and most important group of land plants, with over 250,000 species and a dominating presence in most terrestrial ecosystems. Understanding the origin and early diversification of angiosperms has posed a long-standing botanical challenge [1]. Numerous morphological and molecular systematic studies have attempted to reconstruct the early history of this group, including identifying the root of the angiosperm tree. There is considerable disagreement among these studies, with various groups of putatively basal angiosperms from the subclass Magnoliidae having been placed at the root of the angiosperm tree (reviewed in [2-4]). We investigated the early evolution of angiosperms by conducting combined phylogenetic analyses of five genes that represent all three plant genomes from a broad sampling of angiosperms. Amborella, a monotypic, vessel-less dioecious shrub from New Caledonia, was clearly identified as the first branch of angiosperm evolution, followed by the Nymphaeales (water lillies), and then a clade of woody vines comprising Schisandraceae and Austrobaileyaceae. These findings are remarkably congruent with those from several concurrent molecular studies [5-7] and have important implications for whether or not the first angiosperms were woody and contained vessels, for interpreting the evolution of other key characteristics of basal angiosperms, and for understanding the timing and pattern of angiosperm origin and diversification.