Brian D. Farrell

THE EVOLUTION OF AGRICULTURE IN BEETLES (CURCULIONIDAE: SCOLYTINAE AND PLATYPODINAE)

Abstract Beetles in the weevil subfamilies Scolytinae and Platypodinae are unusual in that they burrow as adults inside trees for feeding and oviposition. Some of these beetles are known as ambrosia beetles for their obligate mutualisms with asexual fungi—known as ambrosia fungi—that are derived from plant pathogens in the ascomycete group known as the ophiostomatoid fungi. Other beetles in these subfamilies are known as bark beetles and are associated with free‐living, pathogenic ophiostomatoid fungi that facilitate beetle attack of phloem of trees with resin defenses. Using DNA sequences from six genes, including both copies of the nuclear gene encoding enolase, we performed a molecular phylogenetic study of bark and ambrosia beetles across these two subfamilies to establish the rate and direction of changes in life histories and their consequences for diversification. The ambrosia beetle habits have evolved repeatedly and are unreversed. The subfamily Platypodinae is derived from within the Scolytinae, near the tribe Scolytini. Comparison of the molecular branch lengths of ambrosia beetles and ambrosia fungi reveals a strong correlation, which a fungal molecular clock suggests spans 60 to 21 million years. Bark beetles have shifted from ancestral association with conifers to angiosperms and back again several times. Each shift to angiosperms is associated with elevated diversity, whereas the reverse shifts to conifers are associated with lowered diversity. The unusual habit of adult burrowing likely facilitated the diversification of these beetle‐fungus associations, enabling them to use the biomass‐rich resource that trees represent and set the stage for at least one origin of eusociality.

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.

IS SPECIALIZATION A DEAD END? THE PHYLOGENY OF HOST USE IN DENDROCTONUS BARK BEETLES (SCOLYTIDAE)

Ecological explanations for the prevalence of resource specialists are abundant, whereas phylogenetic evidence on their origins is scarce. In this paper, we provide a molecular phylogenetic study of the 19 specialist or generalist species in the bark beetle genus Dendroctonus, which collectively attack species in four different genera in the conifer family Pinaceae. Given substantial variation in diet breadth, we asked two general questions concerning the evolution of resource use in this group. How conservative is the evolution of host use in these insects? Does specialization tend to be derived (i.e., a “dead end”)?

Temporal lags and overlap in the diversification of weevils and flowering plants

The extraordinary diversity of herbivorous beetles is usually attributed to coevolution with angiosperms. However, the degree and nature of contemporaneity in beetle and angiosperm diversification remain unclear. Here we present a large-scale molecular phylogeny for weevils (herbivorous beetles in the superfamily Curculionoidea), one of the most diverse lineages of insects, based on ≈8 kilobases of DNA sequence data from a worldwide sample including all families and subfamilies. Estimated divergence times derived from the combined molecular and fossil data indicate diversification into most families occurred on gymnosperms in the Jurassic, beginning ≈166 Ma. Subsequent colonization of early crown-group angiosperms occurred during the Early Cretaceous, but this alone evidently did not lead to an immediate and major diversification event in weevils. Comparative trends in weevil diversification and angiosperm dominance reveal that massive diversification began in the mid-Cretaceous (ca. 112.0 to 93.5 Ma), when angiosperms first rose to widespread floristic dominance. These and other evidence suggest a deep and complex history of coevolution between weevils and angiosperms, including codiversification, resource tracking, and sequential evolution.

The Thoracic Morphology of Archostemata and the Relationships of the Extant Suborders of Coleoptera (Hexapoda)

Thoracic structures of Tetraphalerus bruchi are described in detail. The results were compared with features found in other representatives of Archostemata and other coleopteran suborders. Differences between thoracic structures of Tetraphalerus and members of other archostematan subgroups are discussed. External and internal characters of larval and adult representatives of 37 genera of the coleopteran suborders are outlined, coded and analysed cladistically, with four groups of Neuropterida as outgroup taxa. The results strongly suggest the branching pattern Archostemata + [Adephaga + (Myxophaga + Polyphaga)]. Coleoptera excluding Archostemata are supported with a high Bremer support. Important evolutionary changes linked with this branching event are simplifications of the thoracic skeleton resulting in reduced degrees of freedom (i.e. a restricted movability, especially at the leg bases), and a distinct simplification of the muscle system. This development culminates in Polyphaga, which are also strongly supported as a clade. Internalization of the partly reduced propleura, further muscle losses, and the fusion of the mesoventrites and metaventrites—with reversal in Scirtoidea and Derodontidae—are autapomorphies of Polyphaga. Archostemata is a small relict group in contrast to highly successful xylobiontic groups of Polyphaga. The less efficient thoracic locomotor apparatus, the lack of cryptonephric Malpighian tubules, and the rise of angiosperms with beetle groups primarily adjusted to them may have contributed to the decline of Archostemata.

The beetle tree of life reveals that Coleoptera survived end‐Permian mass extinction to diversify during the Cretaceous terrestrial revolution

Here we present a phylogeny of beetles (Insecta: Coleoptera) based on DNA sequence data from eight nuclear genes, including six single‐copy nuclear protein‐coding genes, for 367 species representing 172 of 183 extant families. Our results refine existing knowledge of relationships among major groups of beetles. Strepsiptera was confirmed as sister to Coleoptera and each of the suborders of Coleoptera was recovered as monophyletic. Interrelationships among the suborders, namely Polyphaga (Adephaga (Archostemata, Myxophaga)), in our study differ from previous studies. Adephaga comprised two clades corresponding to Hydradephaga and Geadephaga. The series and superfamilies of Polyphaga were mostly monophyletic. The traditional Cucujoidea were recovered in three distantly related clades. Lymexyloidea was recovered within Tenebrionoidea. Several of the series and superfamilies of Polyphaga received moderate to maximal clade support in most analyses, for example Buprestoidea, Chrysomeloidea, Coccinelloidea, Cucujiformia, Curculionoidea, Dascilloidea, Elateroidea, Histeroidea and Hydrophiloidea. However, many of the relationships within Polyphaga lacked compatible resolution under maximum‐likelihood and Bayesian inference, and/or lacked consistently strong nodal support. Overall, we recovered slightly younger estimated divergence times than previous studies for most groups of beetles. The ordinal split between Coleoptera and Strepsiptera was estimated to have occurred in the Early Permian. Crown Coleoptera appeared in the Late Permian, and only one or two lineages survived the end‐Permian mass extinction, with stem group representatives of all four suborders appearing by the end of the Triassic. The basal split in Polyphaga was estimated to have occurred in the Triassic, with the stem groups of most series and superfamilies originating during the Triassic or Jurassic. Most extant families of beetles were estimated to have Cretaceous origins. Overall, Coleoptera experienced an increase in diversification rate compared to the rest of Neuropteroidea. Furthermore, 10 family‐level clades, all in suborder Polyphaga, were identified as having experienced significant increases in diversification rate. These include most beetle species with phytophagous habits, but also several groups not typically or primarily associated with plants. Most of these groups originated in the Cretaceous, which is also when a majority of the most species‐rich beetle families first appeared. An additional 12 clades showed evidence for significant decreases in diversification rate. These clades are species‐poor in the Modern fauna, but collectively exhibit diverse trophic habits. The apparent success of beetles, as measured by species numbers, may result from their associations with widespread and diverse substrates – especially plants, but also including fungi, wood and leaf litter – but what facilitated these associations in the first place or has allowed these associations to flourish likely varies within and between lineages. Our results provide a uniquely well‐resolved temporal and phylogenetic framework for studying patterns of innovation and diversification in Coleoptera, and a foundation for further sampling and resolution of the beetle tree of life.

The timing of insect/plant diversification: might Tetraopes (Coleoptera: Cerambycidae) and Asclepias (Asclepiadaceae) have co-evolved?

Ehrlich and Raven’s essay on coevolution has stimulated voluminous work on the mechanisms of insect/plant interaction, but few explicit tests of their model’s prediction that the evolutionary success of entire insect and plant clades is governed by their putative reciprocal adaptations. This paper begins an inquiry into possible coevolutionary diversification for North American milkweeds of the genus Asclepias and one of their few major herbivores, the longhorn beetle genus Tetraopes, focusing first on the historical duration and continuity of the interaction. A phylogeny for Tetraopes and relatives, estimated from morphology and allozymes, shows evident similarity to a morphology based hostplant cladogram synthesized from the literature, though the significance of the correspondence under heuristic statistical tests depends on the treatment of one beetle species reported (without certainty) from multiple host species. Fossils and biogeography support the interpretation that cladogram correspondence reflects synchronous diversification of these two clades, hence opportunity for coevolution, rather than beetle ‘host-tracking’ of previously-diversified plants. Cladogram correspondence is more evident at higher than at lower levels, as expected under Ehrlich and Raven’s model. An apparent phylogenetic progression in the potency and location of milkweed cardenolides, seemingly related to species diversity of both Asclepias and Tetraopes subclades, provides further suggestive evidence for that model. The phylogeography of the Tetraopes/Asclepias assemblage suggests that extant species evolved largely in their current, often quite localized biomes, facilitating potential experimental tests for hypotheses of adaptation and counteradaptation and their importance to diversification.

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

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. Hamiltons 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.

MITONUCLEAR DISCORDANCE IS CAUSED BY RAMPANT MITOCHONDRIAL INTROGRESSION IN NEODIPRION (HYMENOPTERA: DIPRIONIDAE) SAWFLIES

Abstract We investigate the pervasiveness of hybridization and mitochondrial introgression in Neodiprion Rohwer (Hymenoptera; Diprionidae), a Holarctic genus of conifer-feeding sawflies. A phylogenetic analysis of the lecontei species group revealed extensive discordance between a contiguous mitochondrial region spanning three genes (COI, tRNA-leucine, and COII) and three nuclear loci (EF1α, CAD, and an anonymous nuclear locus). Bayesian tests of monophyly and Shimodaira–Hasegawa (SH) tests of topological congruence were consistent with mitochondrial introgression; however, these patterns could also be explained by lineage sorting (i.e., deep coalescence). Therefore, to explicitly test the mitochondrial introgression hypothesis, we used a novel application of coalescent-based isolation with migration (IM) models to measure interspecific gene flow at each locus. In support of our hypothesis, mitochondrial gene flow was consistently higher than nuclear gene flow across 120 pairwise species comparisons (P < 1 × 10−12). We combine phylogenetic and coalescent evidence to identify likely cases of recent and ancient introgression in Neodiprion, and based on these observations, we hypothesize that shared hosts and/or pheromones facilitate hybridization, whereas disparate abundances between hybridizing species promote mitochondrial introgression. Our results carry implications for phylogenetic analysis, and we advocate the separation of high and low gene flow regions to inform analyses of hybridization and speciational history, respectively.