Origin of a haplodiploid beetle lineage

The beetle family Scolytidae includes several groups having regular sib-mating and extremely female-biased sex ratios. Two such groups are known to include haplodiploid species: (i) the tribe Xyleborini and (ii) Coccotrypes and related genera within the tribe Dryocoetini. Relationships of these groups have been controversial. We analysed elongation factor 1-α (852 bp) and cytochrome oxidase 1 (1179 bp) sequences for 40 species. The most-parsimonious trees imply a single origin of haplodiploidy uniting Xyleborini (approximately 1200 species) and sib-mating Dryocoetini (approximately 160 species). The sister-group of the haplodiploid clade is the outcrossing genus Dryocoetes. The controversial genus Premnobius is outside the haplodiploid clade. Most haplodiploid scolytids exploit novel resources, ambrosia fungi or seeds, but a few have the ancestral habit of feeding on phloem. Thus, scolytids provide the clearest example of W. D. Hamilton''s scenario for the evolution of haplodiploidy (life under bark leading to inbreeding and hence to female-biased sex ratios through haplodiploidy) and now constitute a unique opportunity to study diplodiploid and haplodiploid sister-lineages in a shared ancestral habitat. There is some evidence of sex determination by maternally inherited endosymbiotic bacteria, which may explain the consistency with which female-biased sex ratios and close inbreeding have been maintained.     

Evolutionary origins of Gondwanan interactions: How old are Araucaria beetle herbivores?

Studies of a variety of phenomena, ranging from rates of molecular substitution to rates of diversification, draw on estimates of geological age. Studies incorporating estimates of timing from fossils or other geological evidence are largely of relatively young, Tertiary divergences, to which older systems may provide useful comparisons. One apparently old assemblage comprises the beetle groups associated with the ancient genus Araucaria that share comparable, ostensibly Gondwanan distributions with their host. Our previous studies suggested a possibly Cretaceous age for Araucaria associations in bark beetles. However, the absence of confirmed bark beetle fossils earlier than the Tertiary has been taken as evidence of Cretaceous absence, and their confirmed phylogenetic position within the primitively angiosperm-feeding weevil family rules out pre-angiosperm, Jurassic origins. Nevertheless, an early shift from angiosperms to Araucaria seemed plausible in the light of Araucaria fossil history which spans the Mesozoic since the Jurassic. To resolve the phylogenetic affinities and to estimate divergence times of the Australian and South American bark beetle genera affiliated with Araucaria we analysed DNA sequences of nuclear and mitochondrial genes: protein coding elongation factor alpha, enolase and cytochrome oxidase I. The most parsimonious reconstruction of the host relationships of Tomicini from the combined dataset corroborates the ancestral association with the genus Araucaria of both South American and Australian Tomicini. Bayesian estimation of divergence times indicates that the divergence between the Australian and the South American Araucaria-feeding taxa occurred at the very latest in the Cretaceous/Paleocene border and that the age of the first Scolytinae-Araucarsa association would then be during the later stages of the Late Cretaceous, while other known beetle/Araucaria associations are Jurassic.     

The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy

Abstract.— Seed dormancy plays an important role in germination ecology and seed plant evolution. Morphological seed dormancy is caused by an underdeveloped embryo that must mature prior to germination. It has been suggested that the presence of an underdeveloped embryo is plesiomorphic among seed plants and that parallel directional change in embryo morphology has occurred separately in gymnosperms and in angiosperms. We test these hypotheses using original data on embryo morphology of key basal taxa, a published dataset, and the generalized least squares (GLS) method of ancestral character state reconstruction. Reconstructions for embryo to seed ratio (E:S) using family means for 179 families showed that E:S has increased between the ancestral angiosperm and almost all extant angiosperm taxa. Species in the rosid clade have particularly large embryos relative to the angiosperm ancestor. Results for the gymnosperms show a similar but smaller increase. There were no statistically significant differences in E:S between basal taxa and any derived group due to extremely large standard errors produced by GLS models. However, differences between reconstructed values for the angiosperm ancestor and more highly nested nodes are large and these results are robust to topological and branch-length manipulations. Our analysis supports the idea that the underdeveloped embryo is primitive among seed plants and that there has been a directional change in E:S within both angiosperms and gymnosperms. Our analysis suggests that dormancy enforced by an underdeveloped embryo is plesiomorphic among angiosperms and that nondormancy and other dormancy types probably evolved within the angiosperms. The shift in E:S was likely a heterochronic change, and has important implications for the life history of seed plants.     

Nonhost angiosperm volatiles and verbenone disrupt response of western pine beetle, Dendroctonus brevicomis (Coleoptera: Scolytidae), to attractant-baited traps

Nonhost angiosperm volatiles and verbenone were tested for their ability to disrupt the response of western pine beetle, Dendroctonus brevicomis LeConte (Coleoptera: Scolytidae), to attractant-baited multiple funnel traps. Verbenone significantly reduced attraction; however, no difference was observed between 4 and 50 mg/24-h release rates. Combinations of six bark volatiles (benzyl alcohol, benzaldehyde, trans-conophthorin, guaiacol, nonanal, and salicylaldehyde), three green leaf volatiles [(E)-2-hexenal, (E)-2-hexen-1-ol, and (Z)-2-hexen-1-ol], and the nine compounds combined did not significantly reduce D. brevicomis response to attractant-baited traps. However, a significant effect was observed when the bark and green leaf volatiles were combined with verbenone. The nine nonhost angiosperm volatiles (NAVs) significantly augmented the effect of both release rates of verbenone, reducing trap catches to levels significantly below that of either release rate of verbenone alone. trans-Conophthorin, a compound reported to have behavioral activity in a number of other scolytids, was not critical to the efficacy of our NAV blend. Our results suggest that the addition of nonhost angiosperm volatiles to verbenone could be important for developing successful semiochemical-based management techniques for D. brevicomis.     

Multistate characters and diet shifts: evolution of Erotylidae (Coleoptera)

The dominance of angiosperms has played a direct role in the diversification of insects, especially Coleoptera. The shift to angiosperm feeding from other diets is likely to have increased the rate of speciation in Phytophaga. However, Phytophaga is only one of many hyperdiverse lineages of beetles and studies of host-shift proliferation have been somewhat limited to groups that primitively feed on plants. We have studied the diet-diverse beetle family Erotylidae (Cucujoidea) to determine if diet is correlated with high diversification rates and morphological evolution by first reconstructing ancestral diets and then testing for associations between diet and species number and diet and ovipositor type. A Bayesian phylogenetic analysis of morphological data that was previously published in Leschen (2003, Pages 1-108 in Fauna of New Zealand, 47; 53 terminal taxa and 1 outgroup, 120 adult characters and 1 diet character) yielded results that are similar to the parsimony analyses of Leschen (2003). Ancestral state reconstructions based on Bayesian and parsimony inference were largely congruent and both reconstructed microfungal feeding (the diet of the outgroup Biphyllidae) at the root of the Erotylidae tree. Shifts among microfungal, saprophagous, and phytophagous diets were most frequent. The largest numbers of species are contained in lineages that are macrofungal feeders (subfamily Erotylinae) and phytophagous (derived Languriinae), although the Bayesian posterior predictive tests of character state correlation were unable to detect any significant associations. Ovipositor morphology correlated with diet (i.e., acute forms were associated with phytophagy and unspecialized forms were associated with a mixture of diets). Although there is a general trend to increased species number associated with the shift from microfungal feeding to phytophagy (based on character mapping and mainly restricted to shifts in Languriinae), there is a large radiation of taxa feeding on macrofungi. Cycad feeding is scattered in more deeply diverged taxa and may have preceded the evolution of angiosperm feeding in some groups. Preliminary analysis of diet mapped onto higher beetle phylogenies suggests that about half of the major Coleoptera lineages may have had fungus-feeding ancestors. We discuss the roles of stochastic models and prior distributions of the reconstruction of ancestral character states in the context of the current data.     

An aphid lineage maintains a bark‐feeding niche while switching to and diversifying on conifers

Lachnine aphids are unusual among phytophagous insects because they feed on both leafy and woody parts of both angiosperm and conifer hosts. Despite being piercing‐sucking phloem‐feeders, these aphids are most speciose on woody parts of coniferous hosts. To evaluate the significance of this unusual biology on their evolution, we reconstructed the ancestral host and feeding site of the lachnine aphids and estimated important host shifts during their evolution. We sampled 78 species representing 14 of the 18 genera of Lachninae from Asia and North America. We performed parsimony, Bayesian and likelihood phylogenetic analyses of combined mitochondrial Cox1, Cox2, CytB and nuclear EF1a1 DNA sequences. We dated the resulting phylogram's important nodes using Bayesian methods and multiple fossil and secondary calibrations. Finally, we used parsimony and Bayesian ancestral state reconstruction to evaluate ancestral feeding ecology. Our results suggest the lachnine common ancestor fed on a woody part of an angiosperm host in the mid‐Cretaceous. A shift to conifer hosts in the Late Cretaceous is correlated with a subsequent increased diversification in the Palaeogene, but a switch to leafy host tissues did not engender a similar burst of diversification. Extant lachnine lineages exhibit the full range of historical association with their hosts: some appeared before, some concomitant with and some after the appearance of their hosts. We conclude our study by placing all the lachnine genera in five tribes.     

Ambrosia beetle (Coleoptera: Scolytidae) species, flight, and attack on living eastern cottonwood trees

In spring 2002, ambrosia beetles (Coleoptera: Scolytidae) infested an intensively managed 22-ha tree plantation on the upper coastal plain of South Carolina. Nearly 3,500 scolytids representing 28 species were captured in ethanol-baited traps from 18 June 2002 to 18 April 2004. More than 88% of total captures were exotic species. Five species [Dryoxylon onoharaensum (Murayama), Euwallacea validus (Eichhoff), Pseudopityophthorus minutissimus (Zimmermann), Xyleborus atratus Eichhoff, and Xyleborus impressus Eichhoff]) were collected in South Carolina for the first time. Of four tree species in the plantation, eastern cottonwood, Populus deltoides Bartram, was the only one attacked, with nearly 40% of the trees sustaining ambrosia beetle damage. Clone ST66 sustained more damage than clone S7C15. ST66 trees receiving fertilization were attacked more frequently than trees receiving irrigation, irrigation + fertilization, or controls, although the number of S7C15 trees attacked did not differ among treatments. The study location is near major shipping ports; our results demonstrate the necessity for intensive monitoring programs to determine the arrival, spread, ecology, and impact of exotic scolytids.     

Ancestral MADS box genes in Sugi, Cryptomeria japonica D. Don (Taxodiaceae), homologous to the B function genes in angiosperms.

In flowering plants, flower organ identity is controlled by the ABC genes, including several MADS box genes. We present two MADS box genes of a conifer, Cryptomeria japonica D. Don. The genes, CjMADS1 and CjMADS2, were related to the angiosperm B function genes which determine the identities of petals and stamens. A phylogenetic analysis showed that these genes form a new clade outside the angiosperm B group, that is, PISTILLATA (PI) and APETALA3 (AP3) lineages. CjMADS1 had a PI-group specific motif and CjMADS2 had AP3-group specific motifs at the C terminal end, respectively. CjMADS1 was expressed in male strobili (or cones) throughout its development, while CjMADS2 was transiently expressed during male strobilus development. The specific expression in the male reproductive organ indicated that the B function is maintained in gymnosperms. Our cladistic analysis suggests that the gene duplication event which generated B function gene lineages predates the divergence of angiosperms and gymnosperms and that the gene duplication which produced the two genes of C. japonica occurred in an ancestral conifer species.     

Polyploidy and angiosperm diversification

Polyploidy has long been recognized as a major force in angiosperm evolution. Recent genomic investigations not only indicate that polyploidy is ubiquitous among angiosperms, but also suggest several ancient genome-doubling events. These include ancient whole genome duplication (WGD) events in basal angiosperm lineages, as well as a proposed paleohexaploid event that may have occurred close to the eudicot divergence. However, there is currently no evidence for WGD in Amborella, the putative sister species to other extant angiosperms. The question is no longer "What proportion of angiosperms are polyploid?", but "How many episodes of polyploidy characterize any given lineage?" New algorithms provide promise that ancestral genomes can be reconstructed for deep divergences (e.g., it may be possible to reconstruct the ancestral eudicot or even the ancestral angiosperm genome). Comparisons of diversification rates suggest that genome doubling may have led to a dramatic increase in species richness in several angiosperm lineages, including Poaceae, Solanaceae, Fabaceae, and Brassicaceae. However, additional genomic studies are needed to pinpoint the exact phylogenetic placement of the ancient polyploidy events within these lineages and to determine when novel genes resulting from polyploidy have enabled adaptive radiations.     

A novel MADS-box gene subfamily with a sister-group relationship to class B floral homeotic genes

Class B floral homeotic genes specify the identity of petals and stamens during the development of angiosperm flowers. Recently, putative orthologs of these genes have been identified in different gymnosperms. Together, these genes constitute a clade, termed B genes. Here we report that diverse seed plants also contain members of a hitherto unknown sister clade of the B genes, termed B(sister) (B(s)) genes. We have isolated members of the B(s) clade from the gymnosperm Gnetum gnemon, the monocotyledonous angiosperm Zea mays and the eudicots Arabidopsis thaliana and Antirrhinum majus. In addition, MADS-box genes from the basal angiosperm Asarum europaeum and the eudicot Petunia hybrida were identified as B(s) genes. Comprehensive expression studies revealed that B(s) genes are mainly transcribed in female reproductive organs (ovules and carpel walls). This is in clear contrast to the B genes, which are predominantly expressed in male reproductive organs (and in angiosperm petals). Our data suggest that the B(s) genes played an important role during the evolution of the reproductive structures in seed plants. The establishment of distinct B and B(s) gene lineages after duplication of an ancestral gene may have accompanied the evolution of male microsporophylls and female megasporophylls 400-300 million years ago. During flower evolution, expression of B(s) genes diversified, but the focus of expression remained in female reproductive organs. Our findings imply that a clade of highly conserved close relatives of class B floral homeotic genes has been completely overlooked until recently and awaits further evaluation of its developmental and evolutionary importance. Electronic supplementary material to this paper can be obtained by using the Springer Link server located at http://dx.doi.org/10.1007/s00438-001-0615-8.     

A Dendroctonus bark engraving (Coleoptera: Scolytidae) from a middle Eocene Larix (Coniferales: Pinaceae): early or delayed colonization?

An engraving made by a scolytid bark beetle, assigned to the genus Dendroctonus of the tribe Tomicini, has been identified on a mummified, middle Eocene (45 Ma) specimen of Larix altoborealis wood from the Canadian High Arctic. Larix altoborealis is the earliest known species of Larix, a distinctive lineage of pinaceous conifers that is taxonomically identifiable by the middle Eocene and achieved a broad continental distribution in northern North America and Eurasia during the late Cenozoic. Dendroctonus currently consists of three highly host-specific lineages that have pinaceous hosts: a basal monospecific clade on Pinoideae (Pinus) and two sister clades that consist of a speciose clade associated exclusively with Pinoideae and six species that breed overwhelmingly in Piceoideae (Picea) and Laricoideae (Pseudotsuga and Larix). The middle Eocene engraving in L. altoborealis represents an early member of Dendroctonus that is ancestral to other congeneric species that colonized a short-bracted species of Larix. This fossil occurrence, buttressed by recent data on the phylogeny of Pinaceae subfamilies and Dendroctonus species, indicates that there was phylogenetically congruent colonization by these bark-beetle lineages of a Pinoideae + (Piceoideae + Laricoideae) host-plant sequence. Based on all available evidence, an hypothesis of a geochronologically early invasion during the Early Cretaceous is supported over an alternative view of late Cenozoic cladogenesis by bark beetles onto the Pinaceae. These data also suggest that host-plant chemistry may be an effective species barrier to colonization by some bark-beetle taxa over geologically long time scales.     

Conservation and divergence in the AGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events

The MADS-box gene AGAMOUS (AG) plays a key role in determining floral meristem and organ identities. We identified three AG homologs, EScaAG1, EScaAG2, and EScaAGL11 from the basal eudicot Eschscholzia californica (California poppy). Phylogenetic analyses indicate that EScaAG1 and EScaAG2 are recent paralogs within the AG clade, independent of the duplication in ancestral core eudicots that gave rise to the euAG and PLENA (PLE) orthologs. EScaAGL11 is basal to core eudicot AGL11 orthologs in a clade representing an older duplication event after the divergence of the angiosperm and gymnosperm lineages. Detailed in situ hybridization experiments show that expression of EScaAG1 and EScaAG2 is similar to AG; however, both genes appear to be expressed earlier in floral development than described in the core eudicots. A thorough examination of available expression and functional data in a phylogenetic context for members of the AG and AGL11 clades reveals that gene expression has been quite variable throughout the evolutionary history of the AG subfamily and that ovule-specific expression might have evolved more than twice. Although sub- and neofunctionalization are inferred to have occurred following gene duplication, functional divergence among orthologs is evident, as is convergence, among paralogs sampled from different species. We propose that retention of multiple AG homologs in several paralogous lineages can be explained by the conservation of ancestral protein activity combined with evolutionarily labile regulation of expression in the AG and AGL11 clades such that the collective functions of the AG subfamily in stamen and carpel development are maintained following gene duplication.     

Phytochrome gene expression and phylogenetic analysis in the short-day plant Pharbitis nil (Convolvulaceae): Differential regulation by light and an endogenous clock

To investigate the role of distinct phytochrome pools in photoperiodic timekeeping, we characterized four phytochrome genes in the short-day plant Pharbitis nil. Each PHY gene had different photosensory properties and sensitivity to night break that inhibits flowering. During extended dark periods, PHYE, PHYB, and PHYC mRNA accumulation exhibited a circadian rhythmicity indicative of control by an endogenous clock. Phylogenetic analysis recovered four clades of angiosperm phytochrome genes, phyA, phyB, phyC, and phyE. All except the phyE clade included sequences from both monocots and eudicots. In addition, phyA is sister to phyC and phyE sister to phyB, with gymnosperm sequences sister to either the phyA-phyC clade or to the phyB-phyE clade. These results suggest that a single duplication occurred in an ancestral seed plant before the divergence of extant gymnosperms from angiosperms and that two subsequent duplications occurred in an ancestral angiosperm before the divergence of monocots from eudicots. Thus in P. nil, a multigene family with different patterns of mRNA abundance in light and darkness contributes to the total phytochrome pool: one pool is light labile (phyA), whereas the other is light stable (phyB and phyE). In addition, PHYC mRNA represents a third phytochrome pool with intermediate photosensory properties.     

Molecular phylogeny of the plant bugs (Heteroptera: Miridae) and the evolution of feeding habits

The first comprehensive cladistic analysis of Miridae, the plant bugs, is presented based on analysis of 3935 base pairs of mitochondrial (16S, COI) and nuclear (18S, 28SD3) DNA for 91 taxa in seven subfamilies. Data were analysed using maximum likelihood (ML), parsimony and Bayesian inference (BI) phylogenetic frameworks. The phylogenetic results are compared with previous hypotheses of higher relationships in the family using alternative hypothesis tests. A Bayesian relaxed molecular clock is used to examine divergence times, and ancestral feeding habits are reconstructed using parsimony and a Bayesian approach. Clades recovered in all analyses are as follows: Cimicomorpha, Miroidea and Miridae; Bryocorinae: Bryocorini; Stenodemini; Mirinae; Deraeocorinae (Clevinemini + Deraeocorini); Cylapinae; Isometopinae; Bryocorinae: Dicyphini; Orthotylini; Phylinae (Phylini + Pilophorini), and Phylinae as sister group to all the remaining mirid taxa. These results are largely congruent with former hypotheses based on morphological data with respect to the monophyly of various subfamilies and tribes; however, our results indicate that the subfamily Bryocorinae is not monophyletic, as the two tribes, Dicypini and Bryocorini, were separated in the phylogenetic results. Divergence time estimates indicate that the radiation of the Miridae began in the Permian; most genus‐level radiations within subfamilies began in the late Cretaceous, probably in response to the angiosperm radiation. Ancestral feeding state reconstructions based on Bayesian and parsimony inference were largely congruent and both reconstructed phytophagy as the ancestral state of the Miridae. Furthermore, the feeding habits of the common ancestors of Mirinae + Deraeocorinae, Bryocorinae + Cylapinae + Isometopinae + Orthotylinae, and the remaining taxa excluding Phylinae, were inferred as phytophagous. Therefore, at least three shifts from phytophagy or polyphagy to predation occurred within the Miridae. Additionally, based on the mirid host‐plant records, we discovered several trends, such as a strong relationship between host‐plant ranges and a facultative feeding habit. © The Willi Hennig Society 2011.     

Phylogenetic relationships of the enigmatic angiosperm family Podostemaceae inferred from 18S rDNA and rbcL sequence data

The phylogenetic relationships of some angiosperm families have remained enigmatic despite broad phylogenetic analyses of rbcL sequences. One example is the aquatic family Podostemaceae, the relationships of which have long been controversial because of major morphological modifications associated with their aquatic habit. Podostemaceae have variously been associated with Piperaceae, Nepenthaceae, Polygonaceae, Caryophyllaceae, Scrophulariaceae, Rosaceae, Crassulaceae, and Saxifragaceae. Two recent analyses of rbcL sequences suggest a possible sister-group relationship of Podostemaceae to Crassulaceae (Saxifragales). However, the branch leading to Podostemaceae was long, and use of different outgroups resulted in alternative placements. We explored the phylogenetic relationships of Podostemaceae using 18S rDNA sequences and a combined rbcL + 18S rDNA matrix representing over 250 angiosperms. In analyses based on 18S rDNA data, Podostemaceae are not characterized by a long branch; the family consistently appears as part of a Malpighiales clade that also includes Malpighiaceae, Turneraceae, Passifloraceae, Salicaceae, Euphorbiaceae, Violaceae, Linaceae, Chrysobalanaceae, Trigoniaceae, Humiriaceae, and Ochnaceae. Phylogenetic analyses based on a combined 18S rDNA + rbcL data set (223 ingroup taxa) with basal angiosperms as the outgroup also suggest that Podostemaceae are part of a Malpighiales clade. These searches swapped to completion, and the shortest trees showed enhanced resolution and increased internal support compared to those based on 18S rDNA or rbcL alone. However, when Gnetales are used as the outgroup, Podostemaceae appear with members of the nitrogen fixing clade (e.g., Elaeagnaceae, Ulmaceae, Rhamnaceae, Cannabaceae, Moraceae, and Urticaceae). None of the relationships suggested here for Podostemaceae receives strong bootstrap support. Our analyses indicate that Podostemaceae are not closely allied with Crassulaceae or with other members of the Saxifragales clade; their closest relatives, although still uncertain, appear to lie elsewhere in the rosids.     

Host range expansion by British moths onto introduced conifers

Abstract.

• 1 Over 2% of British angiosperm-feeding moths (Lepidoptera) have been recorded feeding on conifers introduced to Britain, and may be undergoing host range expansion.
• 2 We compared some of the life-history traits and ecological characteristics of fifty such species, originally exploiting angiosperms and now recorded feeding on conifers, with those of 400 non-shifting angiosperm-feeding moths, to identify those factors linked with host shifting.
• 3 Shifting species attack a wider range of angiosperms than non-shifting species, their original hosts tend to be woody tress and shrubs, and they hatch from the egg earlier in the year.
• 4 Comparisons with the random control samples suggest that larval feeding habit and overwintering stage are also important (species with less intimate relations with the host plant, and those overwintering as eggs are more likely to shift); these trends persisted when the taxonomic distribution of the shift species was controlled for, though were no longer significant.
• 5 Moth species in habitats and on host plant families which are associated with conifer afforestation in upland Britain are more likely to shift, suggesting that ecological opportunity is an important factor in host range expansion.

     

Evolutionary dynamics of specialisation in herbivorous stick insects

Understanding the evolutionary dynamics underlying herbivorous insect mega‐diversity requires investigating the ability of insects to shift and adapt to different host plants. Feeding experiments with nine related stick insect species revealed that insects retain the ability to use ancestral host plants after shifting to novel hosts, with host plant shifts generating fundamental feeding niche expansions. These expansions were, however, not accompanied by expansions of the realised feeding niches, as species on novel hosts are generally ecologically specialised. For shifts from angiosperm to chemically challenging conifer hosts, generalist fundamental feeding niches even evolved jointly with strong host plant specialisation, indicating that host plant specialisation is not driven by constraints imposed by plant chemistry. By coupling analyses of plant chemical compounds, fundamental and ecological feeding niches in multiple insect species, we provide novel insights into the evolutionary dynamics of host range expansion and contraction in herbivorous insects.