Charles Mitter

Nitrogen in Insects: Implications for Trophic Complexity and Species Diversification

Disparities in nutrient content (nitrogen and phosphorus) between herbivores and their plant resources have lately proven to have major consequences for herbivore success, consumer‐driven nutrient cycling, and the fate of primary production in ecosystems. Here we extend these findings by examining patterns of nutrient content between animals at higher trophic levels, specifically between insect herbivores and predators. Using a recently compiled database on insect nutrient content, we found that predators exhibit on average 15% greater nitrogen content than herbivores. This difference persists after accounting for variation from phylogeny and allometry. Among herbivorous insects, we also found evidence that recently derived lineages (e.g., herbivorous Diptera and Lepidoptera) have, on a relative basis, 15%–25% less body nitrogen than more ancient herbivore lineages (e.g., herbivorous Orthoptera and Hemiptera). We elaborate several testable hypotheses for the origin of differences in nitrogen content between trophic levels and among phylogenetic lineages. For example, interspecific variation in insect nitrogen content may be directly traceable to differences in dietary nitrogen (including dilution by gut contents), selected for directly in response to the differential scarcity of dietary nitrogen, or an indirect consequence of adaptation to different feeding habits. From some functional perspectives, the magnitude rather than the source of the interspecific differences in nitrogen content may be most critical. We conclude by discussing the implications of the observed patterns for both the trophic complexity of food webs and the evolutionary radiation of herbivorous insects.

ESCALATION OF PLANT DEFENSE: DO LATEX AND RESIN CANALS SPUR PLANT DIVERSIFICATION?

Ehrlich and Ravens postulate that rapid diversification follows innovation in plant defense has often been invoked a posteriori for plant lineages of unusual diversity and chemical distinctiveness. The postulate can be more rigorously tested by defining a novel class of defense using chemical and/or anatomical criteria, independent of taxonomic lineage. If multiple plant lineages have evolved the new defense type, then according to the postulate they should be consistently more diverse than their sister groups (of equal age, by definition) when the latter retain the primitive defensive repertoire. Secretory canals are an independently defined, repeatedly evolved feature that functions to protect plants from herbivores and pathogens. The canals might therefore be expected to allow plant radiation in an adaptive zone of reduced herbivory and disease. We have quantified the evidence for this hypothesis by comparing the diversities of lineages that have independently evolved canal systems with their sister groups for as many plant lineages as current taxonomic evidence allows. A sign test showed that canal-bearing lineages have consistently higher diversities than their sister groups (P = .0021). Explanations for this result, other than selective advantage conferred by secretory canals, are examined and provisionally rejected.

A Large-Scale, Higher-Level, Molecular Phylogenetic Study of the Insect Order Lepidoptera (Moths and Butterflies)

Background Higher-level relationships within the Lepidoptera, and particularly within the species-rich subclade Ditrysia, are generally not well understood, although recent studies have yielded progress. We present the most comprehensive molecular analysis of lepidopteran phylogeny to date, focusing on relationships among superfamilies. Methodology / Principal Findings 483 taxa spanning 115 of 124 families were sampled for 19 protein-coding nuclear genes, from which maximum likelihood tree estimates and bootstrap percentages were obtained using GARLI. Assessment of heuristic search effectiveness showed that better trees and higher bootstrap percentages probably remain to be discovered even after 1000 or more search replicates, but further search proved impractical even with grid computing. Other analyses explored the effects of sampling nonsynonymous change only versus partitioned and unpartitioned total nucleotide change; deletion of rogue taxa; and compositional heterogeneity. Relationships among the non-ditrysian lineages previously inferred from morphology were largely confirmed, plus some new ones, with strong support. Robust support was also found for divergences among non-apoditrysian lineages of Ditrysia, but only rarely so within Apoditrysia. Paraphyly for Tineoidea is strongly supported by analysis of nonsynonymous-only signal; conflicting, strong support for tineoid monophyly when synonymous signal was added back is shown to result from compositional heterogeneity. Conclusions / Significance Support for among-superfamily relationships outside the Apoditrysia is now generally strong. Comparable support is mostly lacking within Apoditrysia, but dramatically increased bootstrap percentages for some nodes after rogue taxon removal, and concordance with other evidence, strongly suggest that our picture of apoditrysian phylogeny is approximately correct. This study highlights the challenge of finding optimal topologies when analyzing hundreds of taxa. It also shows that some nodes get strong support only when analysis is restricted to nonsynonymous change, while total change is necessary for strong support of others. Thus, multiple types of analyses will be necessary to fully resolve lepidopteran phylogeny.

GENETIC VARIATION AND HOST PLANT RELATIONS IN A PARTHENOGENETIC MOTH

Ecological genetics is the investigation of the influence of ecological factors on the genetic properties of populations, and the influence of genetic structure on their ecological properties. Ideally, these studies should determine how genetic variation is affected by selection and by the size, dynamics, and degree of subdivision of populations; what ecological factors determine the relative fitness of genotypes; and what effect the genetic composition of a population has on such ecological parameters as its density, stability, and ecological amplitude. Many studies have demonstrated selection in natural populations; indeed, the widespread existence of selection is perhaps the only generalization that can be made about ecological genetics. But most studies are incomplete. A few, such as the analysis of inversion karyotypes in Drosophila pseudoobscura by Dobzhansky

Diversification at the Insect-Plant InterfaceInsights from phylogenetics

and plants and their insect enemies together constitute more than half of all known terrestrial species and are food for most of the rest. Their interaction is probably responsible, directly and indirectly, for much of terrestrial diversity (Ehrlich and Raven 1964). Yet we are only beginning to understand how the diversity of insect-plant assemblages is determined. The phytophagous insects associated with a particular plant taxon form an ecological unit convenient for study, because an herbivore species typically attacks only a few related plants. Considerable study (reviewed in Strong et al. 1984) has yielded little evidence that diversity in such assemblages is limited by interspecific interactions such as competition (but see Jaenike 1990, Zwolfer 1988), once accorded a dominant role in community structure (MacArthur 1972). Reflecting a broader shift from equilibrial to contingent explanations in ecology (Ricklefs and Schluter in

Systematics and evolution of the cutworm moths (Lepidoptera: Noctuidae): evidence from two protein‐coding nuclear genes

Abstract.  A broad molecular systematic survey of Noctuidae was undertaken to test recent hypotheses on the problematic definitions and relationships of the subfamilies, with special emphasis on the ‘trifines.’ An initial hypothesis of noctuid classification to the subtribal level was synthesized from recent reviews, and then sampled as broadly as possible. Concatenated sequences for the nuclear genes elongation factor‐1α (EF‐1α; 1200 bp) and dopa decarboxylase (DDC; 700–1100 bp) were analysed for a total of 146 exemplar species, twice that of a previous study. Trees were estimated using likelihood, distance, and both equally weighted and ‘six‐parameter’ parsimony. Of the 144 possible nodes, bootstrap support (BP) was ≥ 50% for ∼80, and ≥ 80% for ∼60. There was very strong support (BP ≥ 90%) for an ‘L.A.Q.’ clade encompassing nearly all quadrifine noctuids plus Arctiidae and Lymantriidae, decisively rendering Noctuidae paraphyletic. We present a new classification for Noctuoidea in which Noctuidae sensu stricto is restricted to trifines; most quadrifine subfamilies are raised to full families. Within the ‘L.A.Q.’ clade, Aganainae and Herminiinae were strongly grouped, but other relationships were weakly supported, probably due to limited taxon sampling. Nolidae and Euteliinae + Stictopterinae are generally grouped with the ‘L.A.Q.’ clade, but with weak support. All analyses favour the broadest definitions proposed for the trifine clade (our Noctuidae sensu stricto) although support is not strong, except that the exemplar of Eustrotiinae: Eublemmini is placed securely in the ‘L.A.Q.’ clade. Numerous recent proposals for dismantling and recombining the ‘Hampsonian’ traditional trifine subfamilies are strongly supported, most notably a broadly defined ‘true cutworm’ clade (Noctuinae s.l.), encompassing the greater part of the traditional subfamilies Amphipyrinae, Cuculliinae, Hadeninae and Noctuinae s.s. (BP ≥ 95%). Within this clade there is strong support for Apameini s.s.+ Xylenini s.l. and for Noctuinae s.s. and divisions thereof, but little support for monophyly or subdivision of Hadeninae. Noctuinae s.l. invariably are allied with Heliothinae, scattered remnants of the traditional Amphipyrinae, and several smaller groups in a broader ‘pest clade’, albeit with weak support. Relationships among the remaining ‘lower’ trifines are not strongly resolved. Mapping of a preliminary synopsis of species diversities, host use patterns and latitudinal distributions on the phylogeny suggests that the diversification of trifines may have been promoted, to a degree unique among Macrolepidoptera, by the Tertiary expansion of seasonal, open habitats and their associated herbaceous floras.

Evolutionary Patterns of Host Plant Use by Delphacid Planthoppers and Their Relatives

Planthoppers (Homoptera: Fulgoroidea) are found on every continent except Antarctica and in all major biomes, including tropical rainforests, deserts, grasslands, and the arctic tundra (O’Brien and Wilson 1985). The more than 9000 described species are divided into 19 families (O’Brien and Wilson 1985; Wheeler and Wilson 1987). All species of Fulgoroidea are phytophagous, sucking fluids from leaves, stems, roots, or fungal hyphae. There are species which feed on woody plants (both angiosperms and gymnosperms), herbs, ferns, and even fungi (O’Brien and Wilson 1985).

Repeated climate-linked host shifts have promoted diversification in a temperate clade of leaf-mining flies

A central but little-tested prediction of “escape and radiation” coevolution is that colonization of novel, chemically defended host plant clades accelerates insect herbivore diversification. That theory, in turn, exemplifies one side of a broader debate about the relative influence on clade dynamics of intrinsic (biotic) vs. extrinsic (physical-environmental) forces. Here, we use a fossil-calibrated molecular chronogram to compare the effects of a major biotic factor (repeated shift to a chemically divergent host plant clade) and a major abiotic factor (global climate change) on the macroevolutionary dynamics of a large Cenozoic radiation of phytophagous insects, the leaf-mining fly genus Phytomyza (Diptera: Agromyzidae). We find one of the first statistically supported examples of consistently elevated net diversification accompanying shift to new plant clades. In contrast, we detect no significant direct effect on diversification of major global climate events in the early and late Oligocene. The broader paleoclimatic context strongly suggests, however, that climate change has at times had a strong indirect influence through its effect on the biotic environment. Repeated rapid Miocene radiation of these flies on temperate herbaceous asterids closely corresponds to the dramatic, climate-driven expansion of seasonal, open habitats.

A phylogenetic study of the ‘bombycoid complex’ (Lepidoptera) using five protein-coding nuclear genes, with comments on the problem of macrolepidopteran phylogeny

Abstract This study had two aims. First, we tested the monophyly of and relationships within the ‘bombycoid complex’, an assembly of approximately 5300 species postulated by Minet to represent 12 families in three superfamilies, by sequencing five protein‐coding nuclear gene regions (CAD, DDC, enolase, period, wingless; approximately 6750 bp total) in 66 representatives of most of the subfamilies and tribes. Second, we sought initial evidence on the utility of these genes for estimating relationships among Macrolepidoptera more broadly (11 superfamilies total), by adding representatives of eight families from four other superfamilies, and by assessing the phylogenetic information content of the individual genes and partitions thereof. Analysis of the combined data by likelihood and parsimony upholds monophyly for the bombycoid complex and for Bombycoidea sensu stricto (includes Anthelidae, see below), but with weak bootstrap support. Minet’s assignment of Phiditiinae to Bombycoidea rather than to Noctuoidea is strongly upheld, but Anthelidae, placed in Lasiocampoidea by Minet, group securely within Bombycoidea sensu stricto. Within the latter, the basal split segregates a strongly supported ‘BALE’ group [Apatelodinae + (Eupterotidae + (Brahmaeidae + Lemoniidae))]. The remaining families form a consistently but weakly supported clade, within which the basal split segregates the very strongly supported ‘CAPOPEM’ group [Carthaeidae, Anthelidae, Phiditiinae, (Prismostictini + (Endromidae + (Oberthueriini + Mirinidae)))]. The remaining bombycoids are grouped, very weakly, as Sphingidae + (Bombycinae + Saturniidae). All multiply‐sampled families are strongly recovered, in both outgroups and ingroups, except that Bombycidae sensu Minet are rendered decisively polyphyletic. All genes make important contributions to the combined data results, and there is little strong conflict among genes or between synonymous and nonsynonymous change, although two instances of inter‐gene conflict were notable, one in Lasiocampidae and one in Mimallonidae. Overall, about 75% of nodes are strongly supported (i.e. bootstrap value ≥80%). Superfamilies are recovered, but not always strongly, whereas relationships among superfamilies are recovered only weakly and inconsistently; even within the reasonably well‐sampled Bombycoidea sensu stricto, a (to us) surprising number of interfamily relationships remain uncertain. Thus, it seems clear that substantially more genes, plus additional taxon sampling in most superfamilies, will be required to resolve macrolepidopteran phylogeny.

Can Deliberately Incomplete Gene Sample Augmentation Improve a Phylogeny Estimate for the Advanced Moths and Butterflies (Hexapoda: Lepidoptera)?

Abstract This paper addresses the question of whether one can economically improve the robustness of a molecular phylogeny estimate by increasing gene sampling in only a subset of taxa, without having the analysis invalidated by artifacts arising from large blocks of missing data. Our case study stems from an ongoing effort to resolve poorly understood deeper relationships in the large clade Ditrysia ( > 150,000 species) of the insect order Lepidoptera (butterflies and moths). Seeking to remedy the overall weak support for deeper divergences in an initial study based on five nuclear genes (6.6 kb) in 123 exemplars, we nearly tripled the total gene sample (to 26 genes, 18.4 kb) but only in a third (41) of the taxa. The resulting partially augmented data matrix (45% intentionally missing data) consistently increased bootstrap support for groupings previously identified in the five-gene (nearly) complete matrix, while introducing no contradictory groupings of the kind that missing data have been predicted to produce. Our results add to growing evidence that data sets differing substantially in gene and taxon sampling can often be safely and profitably combined. The strongest overall support for nodes above the family level came from including all nucleotide changes, while partitioning sites into sets undergoing mostly nonsynonymous versus mostly synonymous change. In contrast, support for the deepest node for which any persuasive molecular evidence has yet emerged (78–85% bootstrap) was weak or nonexistent unless synonymous change was entirely excluded, a result plausibly attributed to compositional heterogeneity. This node (Gelechioidea + Apoditrysia), tentatively proposed by previous authors on the basis of four morphological synapomorphies, is the first major subset of ditrysian superfamilies to receive strong statistical support in any phylogenetic study. A “more-genes-only” data set (41 taxa×26 genes) also gave strong signal for a second deep grouping (Macrolepidoptera) that was obscured, but not strongly contradicted, in more taxon-rich analyses.