Nonadaptive host-use specificity in tropical armored scale insects.

Most herbivorous insects are diet specialists in spite of the apparent advantages of being a generalist. This conundrum might be explained by fitness trade-offs on alternative host plants, yet the evidence of such trade-offs has been elusive. Another hypothesis is that specialization is nonadaptive, evolving through neutral population-genetic processes and within the bounds of historical constraints. Here, we report on a striking lack of evidence for the adaptiveness of specificity in tropical canopy communities of armored scale insects. We find evidence of pervasive diet specialization, and find that host use is phylogenetically conservative, but also find that more-specialized species occur on fewer of their potential hosts than do less-specialized species, and are no more abundant where they do occur. Of course local communities might not reflect regional diversity patterns. But based on our samples, comprising hundreds of species of hosts and armored scale insects at two widely separated sites, more-specialized species do not appear to outperform more generalist species.

Phylogeny and classification of armored scale insects (Hemiptera: Coccomorpha: Diaspididae).

Armored scale insects (Hemiptera: Coccomorpha: Diaspididae) are major economic pests and are among the world's most invasive species. Here we describe a system of specimen and identification management that establishes a basis for well-vouchered molecular identification. We also present an expanded Bayesian phylogenetic analysis based on concatenated fragments of 4 genetic loci: the large ribosomal subunit (28S), elongation factor-1 alpha (EF-1α), cytochrome oxidase I and II (COI‒II), and the small ribosomal subunit (16S) of the primary endosymbiont, Uzinura diaspidicola (Bacteroidetes: Flavobacteriales). Our sample includes 1,389 individuals, representing 11 outgroup species and at least 311 described and 61 undescribed diaspidid species. The results broadly support Takagi's 2002 classification but indicate that some revisions are needed. We propose a revised classification recognizing 4 subfamilies: Ancepaspidinae Borchsenius, new rank, Furcaspidinae Balachowsky, new rank, Diaspidinae Targioni Tozzetti, and Aspidiotinae Westwood. Within Aspidiotinae, in addition to the existing tribes Aspidiotini Westwood, Parlatoriini Leonardi, Odonaspidini Ferris, Leucaspidini Atkinson, and Smilacicolini Takagi, we recognize as tribes Gymnaspidini Balachowsky, new rank, and Aonidiini Balachowsky, new rank. Within Diaspidinae we recognize the 2 tribes Lepidosaphidini Shimer and Diaspidini Targioni Tozzetti, and within Diaspidini we recognize three subtribes: Diaspidina Targioni Tozzetti, Fioriniina Leonardi, and Chionaspidina Brues Melander. We regard Kuwanaspidina Borchsenius as a junior synonym of Fioriniina, Thysanaspidini Takagi as a junior synonym of Leucaspidini, and Protodiaspidina Takagi and Ulucoccinae Takagi as junior synonyms of Chionaspidina. To clarify the composition of the higher taxa we describe 2 new genera for Australian species heretofore misplaced in the genus Ancepaspis Ferris: Brimblecombia Normark (Aonidiini) and Hendersonaspis Normark (Leucaspidini). We also propose many additional minor modifications to the taxonomy of Diaspididae, including the following new combinations, revived combinations, and replacement names: Aonidia edgerleyi (Mamet), new combination (from Bigymnaspis Balachowsky); Aonidomytilus espinosai Porter, revived combination (from Porterinaspis González); Aspidiotus badius (Brain), new combination (this and the next 5 Aspidiotus species all from Aonidia Targioni Tozzetti); Aspidiotus biafrae (Lindinger), new combination; Aspidiotus chaetachmeae (Brain), new combination; Aspidiotus laticornis (Balachowsky), new combination; Aspidiotus rhusae (Brain), new combination; Aspidiotus sclerosus (Munting), new combination; Brimblecombia asperata (Brimblecombe), new combination (this and the next 5 Brimblecombia species all from Ancepaspis); Brimblecombia longicauda (Brimblecombe), new combination; Brimblecombia magnicauda (Brimblecombe), new combination; Brimblecombia reticulata (Brimblecombe), new combination; Brimblecombia rotundicauda (Brimblecombe), new combination; Brimblecombia striata (Brimblecombe), new combination; Cooleyaspis pseudomorpha (Leonardi), new combination (from Dinaspis Leonardi); Cupidaspis wilkeyi (Howell Tippins), new combination (from Paracupidaspis Howell Tippins); Cupressaspis isfarensis Borchsenius, revived combination (this species, the next 2 species in Cupressaspis Borchsenius, revived genus, and the next 9 species in Diaspidiotus Cockerell all from Aonidia); Cupressaspis mediterranea (Lindinger), revived combination; Cupressaspis relicta (Balachowsky), new combination; Diaspidiotus atlanticus (Ferris), new combination; Diaspidiotus marginalis (Brain), new combination; Diaspidiotus maroccanus (Balachowsky), new combination; Diaspidiotus mesembryanthemae (Brain), new combination; Diaspidiotus opertus (De Lotto), new combination; Diaspidiotus shastae (Coleman), new combination; Diaspidiotus simplex (Leonardi), new combination; Diaspidiotus visci (Hall), new combination; Diaspidiotus yomae (Munting), new combination; Diaspis arundinariae (Tippins Howell), new combination (from Geodiaspis Tippins Howell); Duplachionaspis arecibo (Howell), new combination (this and the next 10 Duplachionaspis MacGillivray species all from Haliaspis Takagi); Duplachionaspis asymmetrica Ferris, revived combination; Duplachionaspis distichlii (Ferris), revived combination; Duplachionaspis litoralis Ferris, revived combination; Duplachionaspis mackenziei McDaniel, revived combination; Duplachionaspis milleri (Howell), new combination; Duplachionaspis nakaharai (Howell), new combination; Duplachionaspis peninsularis (Howell), new combination; Duplachionaspis spartinae (Comstock), revived combination; Duplachionaspis texana (Liu Howell) new combination; Duplachionaspis uniolae (Takagi), new combination; Duplachionaspis mutica (Williams) (from Aloaspis Williams), new combination; Epidiaspis doumtsopi (Schneider), new combination (from Diaspis Costa); Fiorinia ficicola (Takahashi), new combination (from Ichthyaspis Takagi); Fiorinia macroprocta (Leonardi), revived combination (this and the next 2 species of Fiorinia Targioni Tozzetti all from Trullifiorinia Leonardi); Fiorinia rubrolineata Leonardi, revived combination; Fiorinia scrobicularum Green, revived combination; Genaparlatoria pseudaspidiotus (Lindinger), revived combination (from Parlatoria); Greeniella acaciae (Froggatt), new combination (this and the next 4 Greeniella Cockerell species all from Gymnaspis Newstead); Greeniella cassida (Hall Williams), new combination; Greeniella grandis (Green), new combination; Greeniella perpusilla (Maskell), new combination; Greeniella serrata (Froggatt), new combination; Hendersonaspis anomala (Green), new combination (from Ancepaspis); Hulaspis bulba (Munting), new combination (this and the next Hulaspis Hall species both from Andaspis MacGillivray); Hulaspis formicarum (Ben-Dov), new combination; Lepidosaphes antidesmae (Rao in Rao Ferris), new combination (this and the next 19 species all from Andaspis); Lepidosaphes arcana (Matile-Ferrero), new combination; Lepidosaphes betulae (Borchsenius), new combination; Lepidosaphes citricola (Young Hu), new combination; Lepidosaphes conocarpi (Takagi), new combination; Lepidosaphes crawi (Cockerell), revived combination; Lepidosaphes erythrinae Rutherford, revived combination; Lepidosaphes incisor Green, revived combination; Lepidosaphes indica (Borchsenius), new combination; Lepidosaphes kashicola Takahashi, revived combination; Lepidosaphes kazimiae (Williams), new combination; Lepidosaphes laurentina (Almeida), new combination; Lepidosaphes maai (Williams Watson), new combination; Lepidosaphes mackieana McKenzie, revived combination; Lepidosaphes micropori (Borchsenius), new combination; Lepidosaphes punicae Laing, revived combination; Lepidosaphes quercicola (Borchsenius), new combination; Lepidosaphes recurrens (Takagi Kawai), new combination; Lepidosaphes viticis (Takagi), new combination; Lepidosaphes xishuanbannae (Young Hu), new combination; Lepidosaphes giffardi (Adachi Fullaway), new combination (from Carulaspis MacGillivray); Lepidosaphes garciniae (Young Hu), new combination (this and the next 2 species all from Ductofrontaspis Young Hu); Lepidosaphes huangyangensis (Young Hu), new combination; Lepidosaphes jingdongensis (Young Hu), new combination; Lepidosaphes recurvata (Froggatt), revived combination (from Metandaspis Williams); Lepidosaphes ficicola Takahashi, revived combination (this and the next 2 species all from Ungulaspis MacGillivray); Lepidosaphes pinicolous Chen, revived combination; Lepidosaphes ungulata Green, revived combination; Lepidosaphes serrulata (Ganguli), new combination (from Velataspis Ferris); Lepidosaphes huyoung Normark, replacement name for Andaspis ficicola Young Hu; Lepidosaphes tangi Normark, replacement name for Andaspis schimae Tang; Lepidosaphes yuanfeng Normark, replacement name for Andaspis keteleeriae Yuan Feng; Leucaspis ilicitana (Gómez-Menor), new combination (from Aonidia); Lopholeucaspis spinomarginata (Green), new combination (from Gymnaspis); Melanaspis campylanthi (Lindinger), new combination (from Aonidia); Mohelnaspis bidens (Green), new combination (from Fiorinia); Parlatoria affinis (Ramakrishna Ayyar), new combination (this and the next 4 Parlatoria species all from Gymnaspis); Parlatoria ficus (Ramakrishna Ayyar), new combination; Parlatoria mangiferae (Ramakrishna Ayyar), new combination; Parlatoria ramakrishnai (Green), new combination; Parlatoria sclerosa (Munting), new combination; Parlatoria bullata (Green), new combination (from Bigymnaspis); Parlatoria leucaspis (Lindinger), new combination (this and the next species both from Cryptoparlatorea Lindinger); Parlatoria pini (Takahashi), new combination; Parlatoria tangi Normark, replacement name for Parlatoria pini Tang; Pseudoparlatoria bennetti (Williams), new combination (from Parlagena McKenzie); Pseudoparlatoria chinchonae (McKenzie), new combination (from Protodiaspis Cockerell); Pseudoparlatoria larreae (Leonardi), revived combination (from Protargionia Leonardi); Quernaspis lepineyi (Balachowsky), new combination (from Chionaspis); Rhizaspidiotus nullispinus (Munting), new combination (from Aonidia); Rolaspis marginalis (Leonardi), new combination (from Lepidosaphes); Salicicola lepelleyi (De Lotto), new combination (from Anotaspis Ferris); Tecaspis giffardi (Leonardi), new combination (from Dinaspis); Trullifiorinia geijeriae (Froggatt), new combination (from Fiorinia); Trullifiorinia nigra (Lindinger), new combination (from Crypthemichionaspis Lindinger); and Voraspis olivina (Leonardi), new combination (from Lepidosaphes).

A highly resolved food web for insect seed predators in a species-rich tropical forest.

The top-down and indirect effects of insects on plant communities depend on patterns of host use, which are often poorly documented, particularly in species-rich tropical forests. At Barro Colorado Island, Panama, we compiled the first food web quantifying trophic interactions between the majority of co-occurring woody plant species and their internally feeding insect seed predators. Our study is based on more than 200 000 fruits representing 478 plant species, associated with 369 insect species. Insect host-specificity was remarkably high: only 20% of seed predator species were associated with more than one plant species, while each tree species experienced seed predation from a median of two insect species. Phylogeny, but not plant traits, explained patterns of seed predator attack. These data suggest that seed predators are unlikely to mediate indirect interactions such as apparent competition between plant species, but are consistent with their proposed contribution to maintaining plant diversity via the Janzen-Connell mechanism.

The New World Gibbobruchus Pic (Coleoptera, Chrysomelidae, Bruchinae): description of a new species and phylogenetic insights into the evolution of host associations and biogeography.

The seed beetle Gibbobruchus tridentatus Manfio, Jorge & Ribeiro-Costa sp. nov. is described from the Amazon basin in Brazil (Acre) and Ecuador (Napo), and is included in an updated key to the species of Gibbobruchus Pic. This new species and the recently described G. bergamini Manfio & Ribeiro-Costa are incorporated into a phylogenetic reanalysis of the genus and into a comparative analysis of host plant use and biogeography. Species groups previously proposed were supported and the evolutionary history in host plant-use shows Gibbobruchus conserved at tribe level, Cercideae (Caesalpinioideae), with coordination between biogeographic expansion and host genus shifts. Both species, Gibbobruchus tridentatus Manfio, Jorge & Ribeiro-Costa sp. nov. and G. bergamini, were placed within the group scurra (G. tridentatus (G. scurra (G. cavillator+G. bolivianus+G. bergamini))) and supported by one synapomorphy. Additionally, we update geographic distributions and host plant records. Two hosts, Bauhinia argentinensis Burkart and B. tarapotensis Benth. are recorded for the first time as hosts for the genus and for the subfamily.

Phylogenetic analysis reveals positive correlations between adaptations to diverse hosts in a group of pathogen-like herbivores.

A jack of all trades can be master of none-this intuitive idea underlies most theoretical models of host-use evolution in plant-feeding insects, yet empirical support for trade-offs in performance on distinct host plants is weak. Trade-offs may influence the long-term evolution of host use while being difficult to detect in extant populations, but host-use evolution may also be driven by adaptations for generalism. Here we used host-use data from insect collection records to parameterize a phylogenetic model of host-use evolution in armored scale insects, a large family of plant-feeding insects with a simple, pathogen-like life history. We found that a model incorporating positive correlations between evolutionary changes in host performance best fit the observed patterns of diaspidid presence and absence on nearly all focal host taxa, suggesting that adaptations to particular hosts also enhance performance on other hosts. In contrast to the widely invoked trade-off model, we advocate a "toolbox" model of host-use evolution in which armored scale insects accumulate a set of independent genetic tools, each of which is under selection for a single function but may be useful on multiple hosts.

Fossil palm beetles refine upland winter temperatures in the Early Eocene Climatic Optimum.

Eocene climate and associated biotic patterns provide an analog system to understand their modern interactions. The relationship between mean annual temperatures and winter temperatures-temperature seasonality-may be an important factor in this dynamic. Fossils of frost-intolerant palms imply low Eocene temperature seasonality into high latitudes, constraining average winter temperatures there to >8 °C. However, their presence in a paleocommunity may be obscured by taphonomic and identification factors for macrofossils and pollen. We circumvented these problems by establishing the presence of obligate palm-feeding beetles (Chrysomelidae: Pachymerina) at three localities (a fourth, tentatively) in microthermal to lower mesothermal Early Eocene upland communities in Washington and British Columbia. This provides support for warmer winter Eocene climates extending northward into cooler Canadian uplands.

Reliance on pollinators predicts defensive chemistry across tobacco species.

Defensive traits are typically studied in the context of avoiding antagonists, but may also mediate key interactions with mutualists. Plant chemical defences occur in flowers, suggesting pollinators may be agents of selection on defence. We hypothesised that floral defences would deter pollinators, and therefore, pollinators would select for lower defences in outcrossing than self-pollinating species. We measured pollinator reliance and alkaloid levels in 32 greenhouse-grown Nicotiana species. Using a comparative phylogenetic approach, we found significantly lower nectar, floral and leaf nicotine concentrations in outcrossing than selfing species, with a 15-fold decrease in leaf nicotine levels. Nicotine concentrations were positively correlated across tissues, suggesting that selection against floral defences could constrain the evolution of leaf defences. Thus, pollinators could shape the evolution not only of floral defences but also of defences in other tissues where herbivores have traditionally been considered the dominant agent of selection.

A phylogenetic analysis of armored scale insects (Hemiptera: Diaspididae), based upon nuclear, mitochondrial, and endosymbiont gene sequences.

Armored scale insects (Hemiptera: Diaspididae) are among the most invasive insects in the world. They have unusual genetic systems, including diverse types of paternal genome elimination (PGE) and parthenogenesis. Intimate relationships with their host plants and bacterial endosymbionts make them potentially important subjects for the study of co-evolution. Here, we expand upon recent phylogenetic work (Morse and Normark, 2006) by analyzing armored scale and endosymbiont DNA sequences from 125 species of armored scale insect, represented by 253 samples and eight outgroup species. We used fragments of four different gene regions: the nuclear protein-coding gene Elongation Factor 1α (EF1α), the large ribosomal subunit (28S) rDNA, a mitochondrial region spanning parts of cytochrome oxidase I (COI) and cytochrome oxidase II (COII), and the small ribosomal subunit (16S) rDNA from the primary bacterial endosymbiont Uzinura diaspidicola. Maximum likelihood, and Bayesian analyses were performed producing highly congruent topological results. A comparison of two datasets, one with and one without missing data, found that missing data had little effect on topology. Our results broadly corroborate several major features of the existing classification, although we do not find any of the subfamilies, tribes or subtribes to be monophyletic as currently constituted. Using ancestral state reconstruction we estimate that the ancestral armored scale had the late PGE sex system, and it may as well have been pupillarial, though results differed between reconstruction methods. These results highlight the need for a complete revision of this family, and provide the groundwork for future taxonomic work in armored scale insects.

Geographic variation in body size and sexual size dimorphism of a seed-feeding beetle.

Body size of many animals varies with latitude: body size is either larger at higher latitudes (Bergmann's rule) or smaller at higher latitudes (converse Bergmann's rule). However, the causes underlying these patterns are poorly understood. Also, studies rarely explore how sexual size dimorphism varies with latitude. Here we investigate geographic variation in body size and sexual size dimorphism of the seed-feeding beetle Stator limbatus, collected from 95 locations along a 38 degrees range in latitude. We examine 14 variables to test whether clines in environmental factors are adequate to explain geographic patterns of body size. We found that body size and sexual size dimorphism of S. limbatus varied considerably with latitude; beetles were smaller but more dimorphic at lower latitudes. Body size was not correlated with a gradient in mean temperature, contrary to the commonly accepted hypothesis that clines are produced by latitudinal gradients in temperature. Instead, we found that three factors were adequate to explain the cline in body size: clinal variation in host plant seed size, moisture (humidity), and seasonality (variance in humidity, precipitation, and temperature). We also found that the cline in sexual size dimorphism was partially explainable by a gradient in moisture, though moisture alone was not sufficient to explain the cline. Other ecological or environmental variables must necessarily contribute to differences in selection on male versus female body size. The main implications of our study are that the sexes differ in the magnitude of clinal variation in body size, creating latitudinal variation in sexual size dimorphism, and that clines in body size of seed beetles are likely influenced by variation in host seed size, water availability, and seasonality.

Phylogenetic congruence of armored scale insects (Hemiptera: Diaspididae) and their primary endosymbionts from the phylum Bacteroidetes.

Insects in the sap-sucking hemipteran suborder Sternorrhyncha typically harbor maternally transmitted bacteria housed in a specialized organ, the bacteriome. In three of the four superfamilies of Sternorrhyncha (Aphidoidea, Aleyrodoidea, Psylloidea), the bacteriome-associated (primary) bacterial lineage is from the class Gammaproteobacteria (phylum Proteobacteria). The fourth superfamily, Coccoidea (scale insects), has a diverse array of bacterial endosymbionts whose affinities are largely unexplored. We have amplified fragments of two bacterial ribosomal genes from each of 68 species of armored scale insects (Diaspididae). In spite of initially using primers designed for Gammaproteobacteria, we consistently amplified sequences from a different bacterial phylum: Bacteroidetes. We use these sequences (16S and 23S, 2105 total base pairs), along with previously published sequences from the armored scale hosts (elongation factor 1alpha and 28S rDNA) to investigate phylogenetic congruence between the two clades. The Bayesian tree for the bacteria is roughly congruent with that of the hosts, with 67% of nodes identical. Partition homogeneity tests found no significant difference between the host and bacterial data sets. Of thirteen Shimodaira-Hasegawa tests, comparing the original Bayesian bacterial tree to bacterial trees with incongruent clades forced to match the host tree, 12 found no significant difference. A significant difference in topology was found only when the entire host tree was compared with the entire bacterial tree. For the bacterial data set, the treelengths of the most parsimonious host trees are only 1.8-2.4% longer than that of the most parsimonious bacterial trees. The high level of congruence between the topologies indicates that these Bacteroidetes are the primary endosymbionts of armored scale insects. To investigate the phylogenetic affinities of these endosymbionts, we aligned some of their 16S rDNA sequences with other known Bacteroidetes endosymbionts and with other similar sequences identified by BLAST searches. Although the endosymbionts of armored scales are only distantly related to the endosymbionts of the other sternorrhynchan insects, they are closely related to bacteria associated with eriococcid and margarodid scale insects, to cockroach and auchenorrynchan endosymbionts (Blattabacterium and Sulcia), and to male-killing endosymbionts of ladybird beetles. We propose the name "Candidatus Uzinura diaspidicola" for the primary endosymbionts of armored scale insects.

Ecological and evolutionary diversification of the seed beetle genus Stator (Coleoptera: Chrysomelidae: Bruchinae).

Ehrlich and Raven's (1964) hypothesis on coevolution has stimulated numerous phylogenetic studies that focus on the effects of plant defensive chemistry as the main ecological axis of phytophagous insect diversification. However, other ecological features affect host use and diet breadth and they may have very different consequences for insect evolution. In this paper, we present a phylogenetic study based on DNA sequences from mitochondrial and protein-coding genes of species in the seed beetle genus Stator, which collectively show considerable interspecific variation in host affiliation, diet breadth, and the dispersal stage of the seeds that they attack. We used comparative analyses to examine transitions in these three axes of resource use. We argue that these analyses show that diet breadth evolution is dependent upon colonizing novel hosts that are closely or distantly related to the ancestral host, and that oviposition substrate affects the evolution of host-plant affiliation, the evolution of dietary specialization, and the degree to which host plants are shared between species. The results of this study show that diversification is structured by interactions between different selective pressures and along multiple ecological axes.

Interspecific phylogeography of the Stator limbatus species complex: the geographic context of speciation and specialization.

Diversification in phytophagous insects is often attributed to a propensity toward specialization and to a tendency for speciation to be associated with host-shifts. Phylogenetic analysis revealed a sister relationship between the generalist Stator limbatus and the specialist host-shifted Stator beali, providing a system to examine the genealogical and geographic origins of the main processes involved in this diversification: host-shifts, specialization, and reproductive isolation. We examine the interspecific phylogeographic relationships between these species using mitochondrial DNA sequence data. S. beali is derived within S. limbatus, rendering the latter paraphyletic and suggesting a budding process of speciation. The inherent polarity in this genealogical pattern indicates that the specialist habit, clumping oviposition behavior, and distinct genitalia of S. beali are all derived from the ancestral S. limbatus. The phylogeography of S. limbatus also shows strong geographic structure with divergences corresponding to known biogeographic boundaries, indicating that this evolutionary signal has not been erased by the vagaries of history. However, the derivation of S. beali and the evolution of reproductive isolation between the two species does not correspond to these known biogeographic boundaries, as S. beali and its sister clade of S. limbatus are restricted to the same geographic province. The geographic proximity of diversification combined with a divergence time estimated at the beginning of the Pleistocene indicates that speciation likely occurred very rapidly, although further genetic and ecological work is necessary to examine the mode of speciation. This study provides the historical context for ongoing evolutionary, ecological, and quantitative genetic research on the divergence in diet breadth between these species.