Contact Prof. Farrell

Museum of Comparative Zoology
Harvard University
26 Oxford Street
Cambridge, MA 02138
farrellb [at] oeb.harvard.edu
Phone: (617) 496-1057
Fax: (617) 495-5567

Prof. Farrell's CV

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Abstracts for Farrell Lab publications

McKenna, D.D., and Farrell, B.D. 2010. 9-Genes Reinforce the Phylogeny of Holometabola and Yield Alternate Views on the Phylogenetic Placement of Strepsiptera. PLoS ONE 5(7): e11887. doi:10.1371/journal.pone.0011887. pdf

Background: The extraordinary morphology, reproductive and developmental biology, and behavioral ecology of twisted wing parasites (order Strepsiptera) have puzzled biologists for centuries. Even today, the phylogenetic position of these enigmatic ‘‘insects from outer space’’ [1] remains uncertain and contentious. Recent authors have argued for the placement of Strepsiptera within or as a close relative of beetles (order Coleoptera), as sister group of flies (order Diptera), or even outside of Holometabola.

Methodology/Principal Findings: Here, we combine data from several recent studies with new data (for a total of 9 nuclear genes and ,13 kb of aligned data for 34 taxa), to help clarify the phylogenetic placement of Strepsiptera. Our results unequivocally support the monophyly of Neuropteroidea (=Neuropterida + Coleoptera) + Strepsiptera, but recover Strepsiptera either derived from within polyphagan beetles (order Coleoptera), or in a position sister to Neuropterida. All other supra-ordinal- and ordinal-level relationships recovered with strong nodal support were consistent with most other recent studies.

Conclusions/Significance: These results, coupled with the recent proposed placement of Strepsiptera sister to Coleoptera, suggest that while the phylogenetic neighborhood of Strepsiptera has been identified, unequivocal placement to a specific branch within Neuropteroidea will require additional study.

Archibald, S.B., Bossert, W.H., Greenwood, D.R., and Farrell, B.D. 2010. Seasonality, the latitudinal gradient of diversity, and Eocene insects. Paleobiology 36(3), 374–398. pdf

In the modern world, biotic diversity is typically higher in low-latitude tropical regions where there is abundant insolation (light and heat) and low thermal seasonality. Because these factors broadly covary with latitude, separating their possible effects on species diversity is difficult. The Eocene was a much more equable world, however, with low temperature seasonality extending into lower-insolation higher, cooler latitudes, allowing us to test these factors by comparing insect species diversity in (1) modern, temperate, low-insolation, highly seasonal Harvard Forest, Massachusetts, U.S.A., 42u299N; (2) modern, tropical, high-insolation, low-seasonality La Selva, Costa Rica, 10u269N, and; (3) Eocene, temperate, low-insolation, yet low-seasonality McAbee, British Columbia, Canada, above 50uN paleolatitude. We found insect diversity at McAbee to be more similar to La Selva than to Harvard Forest, with high species richness of most groups and decreased diversity of ichneumon wasps, indicating that seasonality is key to the latitudinal diversity gradient. Further, midlatitude Eocene woody dicot diversities at McAbee, Republic (Washington, U.S.A.), and Laguna del Hunco (Argentina) are also high, similar to modern tropical samples, higher than at the modern midlatitude Harvard Forest. Modern correlations between latitude, species diversity, and seasonal climates were established some time after the Eocene.

Catherine Linnen and Brian D. Farrell. 2010. A test of the sympatric host race formation hypothesis in Neodiprion (Hymenoptera: Diprionidae). Proc Roy Soc B. doi:10.1098/rspb.2010.0577 pdf

Theory suggests that sympatric speciation is possible; however, its prevalence in nature remains unknown. Because Neodiprion sawflies are host specialists and mate on their hosts, sympatric speciation via host shifts may be common in this genus. Here, we test this hypothesis using near-complete taxonomic sampling of a species group, comprehensive geographical and ecological data, and multiple comparative methods. Host-use data suggest that host shifts contributed to the evolution of reproductive isolation in Neodiprion and previous work has shown that gene flow accompanied divergence. However, geographical data provide surprisingly little support for the hypothesis that host shifts occurred in sympatry. While these data do not rule out sympatric host race formation in Neodiprion, they suggest that this speciation mode is uncommon in the genus and possibly in nature.

Duane D. McKenna, Andrea S. Sequeira, Adriana E. Marvaldi, and Brian D. Farrell. 2009. Temporal lags and overlap in the diversification of weevils and flowering plant. PNAS 106:7083-7088. doi:10.1073/pnas.0810618106 pdf

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.

Catherine R. Linnen and Brian D. Farrell. 2007. Mitonuclear Discordances is Caused by Rampant Mitochondrial Introgression in Neodiprion (Hymenoptera: Diprionidae) Sawflies. Evolution 61-6: 1417–1438. pdf

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 (EF1, 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.

McKenna D. D. , & B. D. Farrell. 2006. Tropical forests are both evolutionary cradles and museums of leaf beetle diversity. Proceedings of the National Academy of Science. 103 (29): 10947-10951. pdf

The high extant species diversity of tropical lineages of organisms is usually portrayed as a relatively recent and rapid development or as a consequence of the gradual accumulation or preservation of species over time. These explanations have led to alternative views of tropical forests as evolutionary ‘‘cradles’’ or ‘‘museums’’ of diversity, depending on the organisms under study. However, biogeographic and fossil evidence implies that the evolutionary histories of diversification among tropical organisms may be expected to exhibit characteristics of both cradle and museum models. This possibility has not been explored in detail for any group of terrestrial tropical organisms. From an extensively sampled molecular phylogeny of herbivorous Neotropical leaf beetles in the genus Cephaloleia, we present evidence for (i) comparatively ancient Paleocene–Eocene adaptive radiation associated with global warming and Cenozoic maximum global temperatures, (ii) moderately ancient lineage-specific diversification coincident with the Oligocene adaptive radiation of Cephaloleia host plants in the genus Heliconia, and (iii) relatively recent Miocene–Pliocene diversification coincident with the collision of the Panama arc with South America and subsequent bridging of the Isthmus of Panama. These results demonstrate that, for Cephaloleia and perhaps other lineages of organisms, tropical forests are at the same time both evolutionary cradles and museums of diversity.

Nyman, T., A.G. Zinovjev, V. Vikberg, and B.D. Farrell. 2006. Molecular phylogeny of the sawfly family Nemetinae (Hymenoptera: Tenthredinidae). Systematic Entomology 31. 569-583. pdf

Nematinae is one of the largest subfamilies in the sawfly family Tenthredinidae, but internal relationships are unknown in the absence of any formal phylogenetic analysis. To understand the internal phylogeny of Nematinae, we sequenced a portion of the mitochondrial cytochrome oxidase I gene and the nuclear elongation factor-1a gene from thirteen outgroup taxa and sixty-eight nematine species, the ingroup taxa of which represent all major genera and subgenera within the subfamily. Maximum parsimony and Bayesian phylogenetic analyses of the DNA sequence data show that: (1) Nematinae are monophyletic in a broad sense which includes Hoplocampa, Susana and the tribe Cladiini, which have been classified often into separate subfamilies; together with Craterocercus, these taxa form a paraphyletic basal grade with respect to the remaining Nematinae, but among-group relationships within the grade remain weakly resolved; (2) the remainder of the ingroup, Nematinae s. str, is monophyletic in all combined-data analyses; (3) within Nematinae s. str, the ‘Higher’ Nematinae is divided into three groups, Mesoneura and the large tribes Nematini and Pristiphorini; (4) although the traditional classifications at the tribal level are largely upheld, some of the largest tribes and genera are obviously para- or polyphyletic; (5) according to rate-smoothed phylogenies dated with two fossil calibration points, Nematinae originated 50–120 million years ago. In addition, the results from all Bayesian analyses provide strong and consistent support for the monophyly of Tenthredinidae, which has been difficult to demonstrate in previous parsimony analyses of morphological and molecular data.

Nyman, T., B.D. Farrell., A.G. Zinovjev, and V. Vikberg. 2006. Larval habits, host- plant associations, and speciation in Nematine sawflies (Hymenoptera: Tenthredinidae) Evolution 60(8): 1622-1637. pdf

Adaptive radiations consist of two intertwined processes, diversification of species and diversification of their ecological niches, but it is unclear whether there is a causal link between the processes. In phytophagous insects, ecological diversification mainly involves shifts in host-plant associations and in larval feeding habits (internal or external) on different plant parts, and several observations indicate that speciation is facilitated by host shifts. Data on host use in individual species suggest that internal feeders are less likely to colonize new hosts than externalfeeding taxa and, consequently, increases in collective host ranges and species numbers should be slowed down in endophagous lineages. We tested these related hypotheses by using phylogenetic information to reconstruct the evolutionary history of larval resource use in the sawfly subfamily Nematinae, a group of 1000 plus species with a broad range of niches: the subfamily’s combined host range includes over 20 plant families, and larvae may feed externally on leaves or needles, or internally, for example, in buds, fruits, leaves, or galls. The results show that:

  1. Most internally feeding groups have evolved independently from external-feeding ancestors, but several distinct internal habits have appeared convergently multiple times;
  2. Shifts among host taxa are clearly more common than changes in larval habits;
  3. The majority of host switches have occurred among phylogenetically close plant groups, but many shifts are manifest among distantly related, ecologically proximate hosts;
  4. Although external feeding characteristic of the common ancestor of Nematinae is associated with relatively high rates of host-shifting, internal feeders are very conservative in their host use;
  5. In contrast, the effect of endophagy on speciation probabilities is more variable:
    net speciation rates are lowered in most internal-feeding groups, but a striking exception is found in species that induce galls on Salicaceae. The loose connection between collective host ranges and species diversity provides empirical support for theoretical models suggesting that speciation rates are a function of a complex interplay between ‘‘intrinsic’’ niche width and resource heterogeneity.

Smith, C.I. and B.D. Farrell. 2006. Evolutionary consequences of dispersal ability in cactus-feeding insects. Genetica 126: 323-334. pdf

Although gene flow is an important determinant of evolutionary change, the role of ecological factors such as specialization in determining migration and gene flow has rarely been explored empirically. To examine the consequences of dispersal ability and habitat patchiness on gene flow, migration rates were compared in three cactophagous longhorn beetles using coalescent analyses of mtDNA sequences. Analyses of covariance were used to identify the roles of dispersal ability and habitat distribution in determining migration patterns. Dispersal ability was a highly significant predictor of gene flow (p<0.001), and was more important than any other factor. These findings predict that dispersal ability may be an import factor shaping both microevolutionary and macroevolutionary patterns; this prediction is borne out by comparisons of species diversity in cactus-feeding groups.

Eastwood, R., S.L. Boyce and B.D. Farrell. 2006. The provenance of old world swallowtail butterflies, Papilio demoleus (Lepidoptera: Papilionidae), recently discovered in the new World. Ann. Entomol. Soc. Am 99(1): 164-168. pdf

A potential citrus pest, the Old World swallowtail butterfly Papilio demoleus L. was recently discovered in the Dominican Republic; however, there are many subspecies of this butterfly and not all are considered pests of citrus.We used genetic markers to determine the source population (subspecies), by comparing sequences from butterflies collected in the Dominican Republic with individuals whose provenance was known, and to indicate whether single or multiple introductions had taken place. Sequences of up to 1,400 nucleotides from the mitochondrial cytochrome oxidase subunit I gene were characterized from 28 specimens collected in the Dominican Republic and compared with known P. demoleus sequences available from GenBank. We confirmed earlier estimates, based on morphology, that the butterflies had originated in Southeast Asia, where the species is known to be a citrus pest. Lack of sequence variation among specimens from the Dominican Republic suggests that a single introduction in early 2004 was most likely. It is not known how the butterflies reached the Dominican Republic.

Smith, C.I. and B.D. Farrell. 2005. Historical biogeography of longhorn cactus beetles: The influence of Pleistocene climate changes on American desert communities. USDA Forest Service Proceedings RMRS-P-36. 135 -139. pdf

Mitochondrial sequence data from three species of flightless cactus beetles, Moneilema gigas, M. armatum, and M. appressum, were analyzed. The coalescent models implemented in the program FLUCTUATE were used to test the hypothesis that these species experienced range changes following the end of the last glacial period. The two desert species M. gigas and M. armatum both showed significant evidence of population growth, particularly in northern populations; however, the montane species M. appressum did not show evidence of range fragmentation and population decline as predicted from paleoclimate data.

McKenna, D.D. and B.D. Farrell. 2005. Molecular phylogenetics and evolution of host plant use in the Neotropical rolled leaf "hispine" beetle genus Cephaloleia (Chevrolat) (Chrysomelidae: Cassidinae). Molecular Phylogenetics and Evolution. 37: 117-131. pdf

Here, we report the results of a species level phylogenetic study of Cephaloleia beetles designed to clarify relationships and patterns of host plant taxon and tissue use among species. Our study is based on up to 2088 bp of mtDNA sequence data. Maximum parsimony, maximum likelihood, and Bayesian methods of phylogenetic inference consistently recover a monophyletic Cephaloleia outside of a basal clade of primarily palm feeding species (the ‘Arecaceae-feeding clade’), and C. irregularis. In all three analyses, the ‘Arecaceae-feeding clade’ includes Cephaloleia spp. with unusual morphological features, and a few species currently placed in other cassidine genera and tribes. All three analyses also recover a clade that includes all Zingiberales feeding Cephaloleia and most Cephaloleia species (the ‘Zingiberales-feeding clade’). Two notable clades are found within the ‘Zingiberales-feeding clade.’ One is comprised of beetles that normally feed only on the young rolled leaves of plants in the families Heliconiaceae and Marantaceae (the ‘Heliconiaceae & Marantaceae-feeding clade’). The other is comprised of relative host tissue generalist, primarily Zingiberales feeding species (the ‘generalist-feeding clade’). A few species in the ‘generalist-feeding clade’ utilize Cyperaceae or Poaceae as hosts. Overall, relatively basal Cephaloleia (e.g., the ‘Arecaceae clade’) feed on relatively basal monocots (e.g., Cyclanthaceae and Arecaceae), and relatively derived Cephaloleia (e.g., the ‘Zingiberales-feeding clade’) feed on relatively derived monocots (mostly in the order Zingiberales). Zingiberales feeding and specialization on young rolled Zingiberales leaves have each apparently evolved just once in Cephaloleia.

Smith, C. I. and B.D. Farrell. 2005. Phylogeography of the longhorn cactus beetle Moneilema appressum Leconte (Coleoptera: Cerambycidae): Was the differentiation of the Madrean sky-islands driven by Pleistocene climate changes?. Molecular Ecology. 14: 3049-3065. pdf

Although it has been suggested that Pleistocene climate changes drove population differentiation and speciation in many groups of organisms, population genetic evidence in support of this scenario has been ambiguous, and it has often been difficult to distinguish putative vicariance from simple isolation by distance. The sky island communities of the American Southwest present an ideal system in which to compare late Pleistocene range fragmentations documented by palaeoenvironmental studies with population genetic data from organisms within these communities. In order to elucidate the impact of Pleistocene climate fluctuations on these environments, biogeographic patterns in the flightless longhorn cactus beetle, Moneilema appressum were examined using mitochondrial DNA sequence data. Gene tree relationships between haplotypes were inferred using parsimony, maximum-likelihood, and Bayesian analysis. Nested clade analysis, Mantel tests, and coalescent modelling were employed to examine alternative biogeographic scenarios, and to test the hypothesis that Pleistocene climate changes drove population differentiation in this species. The program MDIV was used to estimate migration and divergence times between populations, and to measure the statistical support for isolation over ongoing migration. These analyses showed significant geographic structure in genetic relationships, and implicated topography as a key determinant of isolation. However, although the coalescent analyses suggested that a history of past habitat fragmentation underlies the observed geographic patterns, the nested clade analysis indicated that the pattern was consistent with isolation by distance. Estimated divergence times indicated that range fragmentation in M. appressum is considerably older than the end of the most recent glacial, but coincided with earlier interglacial warming events and with documented range expansions in other, desert-dwelling species of Moneilema.

Smith, C. I., and B. D. Farrell. 2005. Range expansion in flightless longhorn cactus beetles Moneilema gigas and M. armatum in response to Pleistocene climate changes. Molecular Ecology 14: 1025-1044. pdf

Pollen cores and plant and animal fossils suggest that global climate changes at the end of the last glacial period caused range expansions in organisms indigenous to the North American desert regions, but this suggestion has rarely been investigated from a population genetic perspective. In order to investigate the impact of Pleistocene climate changes and glacial/interglacial cycling on the distribution and population structure of animals in North American desert communities, biogeographical patterns in the flightless, warm-desert cactus beetles, Moneilema gigas and Moneilema armatum, were examined using mitochondrial DNA(mtDNA) sequence data from the cytochrome oxidase I (COI) gene. Gene tree relationships between haplotypes were inferred using parsimony, maximum-likelihood, and Bayesian analysis. Nested clade analysis and coalescent modelling using the programs MDIV and FLUCTUATE were used to identify demographically independent populations, and to test the hypothesis that Pleistocene climate changes caused recent range expansions in these species. A sign test was used to evaluate the probability of observing concerted population growth across multiple, independent populations. The phylogeographical and nested clade analyses reveal a history of northward expansion in both of these species, as well as a history of past range fragmentation, followed by expansion from refugia. The coalescent analyses provide highly significant evidence for independent range expansions from multiple refugia, but also identify biogeographical patterns that predate the most recent glacial period. The results indicate that widespread desert environments are more ancient than has been suggested in the past.

Morse, G. E., and B. D. Farrell. 2005. Interspeciec phylogeography of the Stator limbatus species complex: The geographic context of speciation and specialization. Molecular Phylogenetics and Evolution 36 (2005) 201–213. pdf

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 diversiWcation: host-shifts, specialization, and reproductive isolation. We examine the interspeciWc 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.

Morse, G. E., and B. D. Farrell. 2005. Ecological and evolutionary diversification of the seed beetle genus Stator. Evolution 59: 1315- 1333. pdf

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.

Lefevre, C., H. Charles, A. Vallier, B. Delobel, B. Farrell, and A. Heddi. 2004. Endosymbiont phlyogenesis in the Dryophthoridae weevils: Evidence for bacterial replacement. Molecular Biology and Evolution 21: 965-973. pdf

Intracellular symbiosis is widespread in the insect world where it plays an important role in evolution and adaptation. The weevil family Dryophthoridae (Curculionoidea) is of particular interest in intracellular symbiosis evolution with regard to the great economical and ecological features of these invasive insects, and the potential for comparative studies across a wide range of host plants and environments. Here, we have analyzed the intracellular symbiotic bacteria of 19 Dryophthoridae species collected worldwide, representing a wide range of plant species and tissues. All except one (Sitophilus linearis) harbor symbiotic bacteria within specialized cells (the bacteriocytes) assembled as an organ, the bacteriome. Phylogenetic analysis of the 16S rDNA gene sequence of the Dryophthoridae endosymbionts revealed three endosymbiotic clades belonging to gamma3-Proteobacteria and characterized by different GC contents and evolutionary rate. The genus name Candidatus Nardonella was proposed for the ancestral clade infesting Dryophthoridae 100 MYA and represented by five of nine bacterial genera studied. For this clade showing low GC content (40.5% GC) and high evolutionary rate (0.128 substitutions/site per 100 Myr), a single infection and subsequent cospeciation of the host and the endosymbionts was observed. In the two other insect lineage endosymbionts, with relatively high GC content (53.4% and 53.8% GC), competition with ancestral pathogenic bacteria might have occurred, leading to endosymbiont replacement in present-day last insects.

Guerrero, K. A., D. Veloz, S. L. Boyce, and B. D. Farrell. 2004. First New World documentation of an Old World citrus pest, the Lime Swallowtail Papilio demoleus (Lepidoptera: Papilionidae), in the Dominican Republic (Hispaniola). American Entomologist 50:224-226. pdf

Papilio demoleus L., a well-known citrus pest in the Old World, is documented from eastern Dominican Republic on the Caribbean island of Hispaniola. Resumen. Se registra la especie Papilio demoleus, una reconocido plaga de los citricos en el Mundo Viejo, para la Hispaniola Republica Dominicana. KEY WORDS: West Indies, Hispaniola, distribution, Lepidoptera, Papilionidae, Papilio demoleus, invasive species, citrus pest.

Farrell, B. D., and A. S. Sequeira. 2004. Evolutionary rates in the adaptive radiation of beetles on plants. Evolution 58:1984-2001. pdf

Herbivorous insects and other small consumers are often specialized both in use of particular host taxa and in use of particular host tissues. Such consumers also often seem to show consistent differences in the rates of evolution of these two dimensions of host use, implying common processes, but this has been little studied. Here we quantify these rates of change in host use evolution in a major radiation of herbivorous insects, the Chrysomeloidea, whose diversity has been attributed to their use of flowering plants. We find a significant difference in the rates of evolutionary change in these two dimensions of host use, with host taxon associations most labile. There are apparently similar differences in rates of host use evolution in other parasite groups, suggesting the generality of this pattern. Divergences in parasite form associated with use of different host tissues may facilitate resource partitioning among successive adaptive radiations on particular host taxa.

Archibald, S. B., and B. D. Farrell. 2003. Wheeler's Dilemma: Proceedings of the Second Paleoentomological Congress. Acta Zoologica Cracoviensia 46 (Supplement-Fossil Insects):17-23. pdf

We identify certain biota as "tropical" and others as "temperate" in the modern world, yet this distinction was not as clear in the early Tertiary. Indeed, many authors have commented upon the well-documented co-occurence of tropical and temperate biotas in the early Tertiary deposits; REID and CHANDLER (1933) called this "one of tte most vexed of climatological problems." Almost a century ago, William Morton Wheeler (1910) noted the surprising mix of warm and cool-adapted ant genera found together in Baltic amber. We review some other warm/cool assemblages of insects, plants, and vertebrates, which occur at Eocene extra-tropical localities worldwide. Explanantions of time averaging, transitional assemblages between climatic regimes and mixing of biocoenoses are unsatisfying. Instead, these seemingly anomolous mixtures are consistent with hypothesized low temperature seasonality in early Tertiary temperate regions. The sorting of biota into temperate and tropical-identified may be a later Cenozoic phenomenon that reflects our specific modern climatic regime of high seasonality in extra tropical regions, rather than an innate and historical biogeographic association of the organisms with their present latitudinal ranges. Thus, the presence of clearly thermophilic organisms outside of low latitudes in early Tertiary assemblages may indicate milder winters, not necessarily tropical or subtropical climate.

Pereira, G., H. De Stefano, J. Staton, and B. D. Farrell. 2002. Phylogenetic relationships among species of Macrobrachium based on sequences of the mitochondrial gene cytochrome oxidase subunit 1. Pages 319-322 in Modern Approaches to the Study of Crustacea (E. Escobar-Briones, and F. Alvarez, eds.). Kluwer Academic Press/Plenum Publishers, New York. pdf

A phylogeny for four species of the freshwater 1 prawn genus Macrobrachiurn (M. carcinus, M, oyetsii, M. ucunthum and M. rosenbeugii) based on the partial nucleotide sequence of the mitochondr~alc ytochrome c oxidase subunlt 1 gene IS presented. The results are consistent wth 1 previous studies based on morphological data

Marvaldi, A. E., A. S. Sequeira, C. W. O'Brien, and B. D. Farrell. 2002. Molecular and morphological phylogenetics of weevils (Coleoptera: Curculionoidea): Do niche shifts accompany diversification? Systematic Biology 51:761-785. pdf

The main goals of this study were to provide a robust phylogeny for the families of Curculionoidea, to discover relationships and major natural groups within the family Curculionidae, and to clarify the evolution of larval habits and host-plant associations in weevils in order to analyse their role in weevil diversification. Phylogenetic relationships among the weevils (Curculionoidea) were inferred from cladistic analysis of nucleotide sequences of 18S ribosomal DNA (~2,000 bases) and 115 morphological characters of larval and adult stages. A worldwide sample of 100 species was made to maximize representation of weevil morphological and ecological diversity. All families and the main subfamilies of Curculionoidea are represented: Nemonychidae (Rhinorhynchinae, Cimberidinae), Anthribidae (Anthribinae), Belidae (Belinae, Oxycoryninae), Attelabidae (Attelabinae, Rhynchitinae), Caridae (Carinae), Brentidae ( Eurhynchinae, Cyladinae, Ithycerinae, Antliarhininae, Apioninae), and Curculionidae sensu lato. The latter family is represented by about 80 species in 30 "subfamilies" of traditional classifications (e g. Erirhininae, Dryophthorinae, Entiminae, Curculioninae, Molytinae, Cossoninae, Scolytinae, Platypodinae, etc.). Three species of Chrysomeloidea were included as outgroups. Phylogenetic reconstruction was done by parsimony analysis of separate and combined molecular and morphological data matrices, and also by bayesian analysis of the molecular data; tree topology support was evaluated, and incongruence between molecular and morphological data sets was tested. Results of the combined analysis of 18S/morphology show that monophyly of, and relationships among, each of the weevil families are well supported with the topology ((Nemonychidae Anthribidae) (Belidae (Attelabidae (Caridae (Brentidae Curculionidae))))). Within the clade Curculionidae sensu lato the basal positions are occupied by (mostly monocot-associated) taxa with the "primitive" type of male genitalia, followed by the Curculionidae sensu stricto, made up of groups with the "derived" type of male genitalia. High support values were found for the monophyly of some distinct curculionid groups like the Dryophthorinae (several tribes represented) and the Platypodinae (Tesserocerini plus Platypodini), among others. However, the subfamilial relationships in Curculionidae are unresolved or weakly supported. The phylogeny estimate based on 18S/morphology suggests that diversification in weevils is accompanied by niche shifts in host plant associations and in larval habits. Pronounced conservatism is shown in larval feeding habits, particularly in the host tissue consumed. Multiple shifts to use of angiosperms in Curculionoidea were identified, each time associated with increases in weevil diversity, and subsequent shifts back to gymnosperms, particularly in the Curculionidae.

Jordal, B. H., R. A. Beaver, B. B. Normark, and B. Farrell. 2002. Extraordinary sex ratios and the evolution of male neoteny in sib-mating Ozopemon beetles. Biological Journal of the Linnean Society 75:353-360. pdf

The weevil subfamily Scolytinae includes at least seven groups of regularly sib-mating species with extremely female-biased offspring sex ratios. The enigmatic SE-Asian bark beetle genus Ozopemon (25 spp.) belong to the most diversified clade (>1400 spp.) of such ancient inbreeding lineages. While males of all sib-mating scolytines are flightless, and are usually dwarfed versions of their larger sisters, the existence of males in Ozopemon has been a controversial issue. Some strangely modified male beetles, with fully developed aedeagus, strongly flattened pronotum and bead, and 10-segmented larviform abdomen, were first described as males of O.brownei, but were later assigned to the Histeridae. With the new evidence provided here, based on DNA sequence data from mitochondrial and nuclear gene partitions, and examination of genitalic characters, we re-assign these males, as well as males for two more species, to Ozopemon. Neoteny evolved close to the origin of sib-mating and possibly haplodiploidy, but the transition to neoteny occurred separately from all other inbreeding dryocoetine and xyleborine beetles. The neotenic development of these males is the first known example in Coleoptera, and several remarkable morphological modifications demonstrate an ontogenetic transformation series from female to males of different species. We discuss possible scenarios for the evolution of neoteny, precocity and fighting characteristics in these male beetles, in the light of W. D. Hamilton's 'ideal biofacies' of extreme inbreeding.

Jordal, B. H., B. B. Normark, B. D. Farrell, and L. R. Kirkendall. 2002. Extraordinary haplotype diversity in haplodiploid inbreeders: phylogenetics and evolution of the bark beetle genus Coccotrypres. Molecular Phylogenetics and Evolution 23:171-188. pdf

Regular inbreeding by sib-mating is one of the most successful ecological strategies in the bark beetle family Scolytinae. Within this family, the many species (119) in Coccotrypes are found breeding in an exceptional variety of untraditional woody tissues different from bark and phloem. Species delineation by morphological criteria is extremely difficult, however, as in most other inbreeding groups of beetles, perhaps due to the unusual evolutionary dynamics characterizing sib-mating organisms. Hence, we here performed a phylogenetic analysis using molecular data in conjunction with morphological data to better understand morphological and ecological evolution in this sib-mating group. We used partial DNA sequences from the nuclear gene EF-alpha and the mitochondrial genes 12S and CO1 to elucidate patterns of morphological evolution, haplotype variation, and evolutionary pathways in resource use. Sequence variation was high among species and far above that expected at the species level (e.g., 19% for CO1 within Coccotrypes advena). The tendency for exhaustive sequence variation at deeper nodes resulted in ambiguous reconstructions of the deepest splits. However, all results suggested that species with the broadest diets were clustered in a single derived position-another piece of evidence against specialization as a derived evolutionary feature.

Sequeira, A. S., and B. D. Farrell. 2001. Evolutionary origins of Gondwanan interactions: How old are Araucaria beetle herbivores? Biological Journal of the Linnean Society 74:459-474. pdf

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–Araucaria association would then be during the later stages of the Late Cretaceous, while other known beetle/Araucaria associations are Jurassic.

Farrell, B. D. 2001. Evolutionary assembly of milkweed fauna: Cytochrome oxidae I and the age of Tetraopes beetles. Molecular Phylogenetics and Evolution 18:467-478. pdf

The insects that feed on the related plant families Apocynaceae and Asclepiadaceae (here collectively termed "milkweeds") comprise a "component community" of highly specialized, distinctive lineages of species that frequently sequester toxic cardiac glycosides from their host plants for defense against predators and are thus often aposematic, advertising their consequent unpalatability. Such sets of specialized lineages provide opportunities for comparative studies of the rate of adaptation, diversification, and habitat-related effects on molecular evolution. The cerambycid genus Tetraopes is the most diverse of the new world milkweed herbivores and the species are generally host specific, being restricted to single, different species of Asclepias, more often so than most other milkweed insects. Previous work revealed correspondence between the phylogeny of these beetles and that of their hosts. The present study provides an alyses of near-complete DNA sequences for Tetraopes and relatives that are used to establish a molecular clock and temporal framework for Tetraopes evolution with their milkweed hosts.

Farrell, B. D., A. S. Sequeira, B. O'Meara, B. B. Normark, J. H. Chung, and B. H. Jordal. 2001. The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55:2011-2027. pdf

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.

Sequeira, A. S., A. A. Lanteri, M. A. Scataglini, V. A. Congalonieri, and B. D. Farrell. 2000. Are flightless Galapaganus weevils older than the Galapagos Islands they inhabit? Heredity 85:20-29. pdf

The 15 species in the weevil genus Galapaganus Lanteri 1992 (Entiminae: Curculionidae: Coleoptera) are distributed on coastal Peru and Ecuador and include 10 flightless species endemic to the Galapagos islands. These beetles thus provide a promising system through which to investigate the patterns and processes of evolution on Darwin's archipelago. Sequences of the mtDNA locus encoding cytochrome oxidase subunit I (COI) were obtained from samples of seven species occurring in different ecological zones of the oldest south-eastern islands: San Cristobal, Espanola and Floreana, and the central island Santa Cruz. The single most parsimonious tree obtained shows two well-supported clades that correspond to the species groups previously defined by morphological characters. Based on a mtDNA clock calibrated for arthropods, the initial speciation separating the oldest species, G. galapagoensis (Linell) on the oldest island, San Cristobal, from the remaining species in the Galapagos occurred about 7.2 Ma. This estimate exceeds geological ages of the extant emerged islands, although it agrees well with molecular dating of endemic Galapagos iguanas, geckos and lizards. An apparent explanation for the disagreement between geological and molecular time-frames is that about 7 Ma there were emerged islands which subsequently disappeared under ocean waters. This hypothesis has gained support from the recent findings of 11-Myr-old submarine seamounts (sunken islands), south-east of the present location of the archipelago. Some species within the darwini group may have differentiated on the extant islands, 1-5 Ma.

Sequeira, A. S., B. B. Normark, and B. D. Farrell. 2000. Evolutionary assembly of the conifer fauna: Distinguishing ancient from recent associations in bark beetles. Proceedings of the Royal Society Biological Series B 267:2359-2366. pdf

Several shifts from ancestral conifer feeding to angiosperm feeding have been implicated in the unparalleled diversification of beetle species. The single largest angiosperm-feeding beetle clade occurs in the weevils, and comprises the family Curculionidae and relatives. Most authorities confidently place the bark beetles (Scolytidae) within this radiation of angiosperm feeders. However, some clues indicate that the association between conifers and some scolytids, particularly in the tribe Tomicini, is a very ancient one. For instance, several fragments of Gondwanaland (South America, New Caledonia, Australia and New Guinea) harbour endemic Tomicini specialized on members of the formerly widespread and abundant conifer family Araucariaceae. As a first step towards resolving this seeming paradox, we present a phylogenetic analysis of the beetle family Scolytidae with particularly intensive sampling of conifer-feeding Tomicini and allies. We sequenced and analysed elongation factor 1-alpha and nuclear rDNAs 18S and 28S for 45 taxa, using members of the weevil family Cossoninae as an out-group. Our results indicate that conifer feeding is the ancestral host association of scolytids, and that the most basal lineages of scolytids feed on Araucaria. If scolytids are indeed nested within a great angiosperm-feeding clade, as many authorities have held, then a reversion to conifer feeding in ancestral scolytids appears to have occurred in the Mesozoic, when Araucaria still formed a major component of the woody flora.

Kelley, S. T., B. D. Farrell, and J. B. Mitton. 2000. Effects of specialization of genetic differentiation is sister species of bark beetles. Heredity 84:218-227. pdf

We investigated the relative importance of resource use and geography on genetic differentiation in the sister-species pair of generalist and specialist bark beetles: Dendroctonus ponderosae and D. jeffreyi (Coleoptera: Scolytidae). In two regions, where the distributions of these species overlap, we collected specimens of the generalist from multiple host species and specimens of the specialist from its single host species. Using allozyme techniques, we uncovered genetic differentiation between generalist populations on different host species in the same region (one locus in each region). However, a much stronger pattern of differentiation was found between specialist populations in the two distantly separated regions (three loci). With mtDNA, we found no significant differentiation between regions in the specialist, or among host species in the generalist, although there was some differentiation between regions in the generalist (AMOVA, P < 0.05). Overall, the generalist populations maintained approximately 10 times the genetic variation in mtDNA as the specialist populations, which suggests that the specialist either has generally smaller population sizes than the generalist, or has experienced a historical population bottleneck.

Jordal, B. H., B. B. Normark, and B. D. Farrell. 2000. Evolutionary radiation of an inbreeding haplodiploid beetle lineage (Curculionidae, Scolytinae). Biological Journal of the Linnean Society 71:483-499. pdf

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-alpha (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 dearest 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 diplo-diploid 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.

Normark, B. B., B. H. Jordal, and B. D. Farrell. 1999. Origin of a haplodiploid beetle lineage. Proceedings of the Royal Society Biological Series B 266:2253-2259. pdf

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-alpha (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.

Dobler, S., and B. D. Farrell. 1999. Host use evolution in Chrysochus milkweed beetles: Evidence from behaviour, population genetics and phylogeny. Molecular Ecology 8:1297-1307. pdf

In two sister species of leaf beetles with overlapping host associations, Chrysochus auratus and C. cobaltinus, we established diet breadth and food preference of local populations for evaluation together with genetic differentiation between populations. While C. auratus turned out to be monophagous on the same plant wherever we collected the beetles, the studied populations of C. cobaltinus fed on three different plant species in the field. Plant preference and ranking of the potential host plants significantly differed between these populations. The amount of genetic differentiation between populations was measured by a polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) assay of a 1300 bp mitochondrial DNA (mtDNA) sequence. In addition, the dominant genotypes of all populations were sequenced. No genetic differentiation between the populations of C. auratus could be detected in the RFLP assay and sequence divergence was low (= 0.3%). In C. cobaltinus, on the other hand, genetic differentiation between populations was high, revealing a lack of gene flow over a much smaller scale and a maximum of 1.3% sequence divergence. C. cobaltinus thereby has the prerequisites for host race formation on different plants from the original host spectrum. Our sequence-based phylogeny estimate allows us to reconstruct historical diet evolution in Chrysochus. Starting from an original association with Asclepiadaceae, the common ancestor of C. auratus and C. cobaltinus included Apocynaceae in its diet. The strict specialization on Apocynum and the loss of acceptance of Asclepiadaceae observed in C. auratus could have resulted from a process similar to that displayed by C. cobaltinus populations.

Kelley, S. T., and B. D. Farrell. 1998. Is specialization a dead end? The phylogeny of host use in Dendroctonus bark beetles (Scolytidae). Evolution 52:1731-1743. pdf

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")? To answer these questions, we estimated the phylogeny of Dendroctonus using mitochondrial DNA sequences and mapped transitions in resource use on the resulting phylogeny estimate. The evolution of affiliations with Pinus and Picea hosts in Dendroctonus was conservative among beetle species (PTP test; P < 0.012), but there was no significant correspondence between the phylogeny of these beetles and the phylogeny among their Pinaceae hosts (among genera, P = 0.28; among Pinus species, P = 0.82). Degree of specialization, as measured in the proportion of hosts used, was bimodally distributed with "generalist" species utilizing gtoreq 60% of the congeneric hosts within their range and six specialist species utilizing ltoreq 40% of the available hosts. Among the generalists, we found a strong correlation between the number of hosts encountered and the number of hosts utilized (R = 0.97, P < 0.0001), whereas there was no significant correlation among the specialists (R = 0.27, P = 0.59). The evolution of specialization in Dendroctonus proved highly labile-specialists arose from generalists at least six separate times (without reversal) all in derived positions, and closer examination of some specialists revealed instances where they appear to have lost particular host species from their diet. However, evidence from the ecological literature also suggests that several Dendroctonus generalists may have increased their range of host genera within the Pinaceae.

Farrell, B. D., and C. Mitter. 1998. The timing of insect/plant diversification: Might Tetraopes (Coleoptera: Cerambycidae) and Asclepias (Asclepiadaceae) have co-evolved? Biological Journal of the Linnean Society 64:553-577. pdf

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.

Farrell, B. D. 1998. "Inordinate fondness" explained: Why are there so many beetles? Science 281:553-557. pdf

The phylogeny of the Phytophaga, the largest and oldest radiation of herbivorous beetles, was reconstructed from 115 complete DNA sequences for the 18S nuclear ribosomal subunit and from 212 morphological characters. The results of these analyses were used to interpret the role of angiosperms in beetle diversification. Jurassic fossils represent basal lineages that are still associated with conifers and cycads. Repeated origins of angiosperm-feeding beetle lineages are associated with enhanced rates of beetle diversification, indicating a series of adaptive radiations. Collectively, these radiations represent nearly half of the species in the order Coleoptera and a similar proportion of herbivorous insect species.

Farrell, B. D., and C. Mitter. 1994. Adaptive radiations in insects and plants: Time and opportunity. American Zoologist 34:57-69. pdf

The spectacular diversity of insects has often been attributed to accelerated radiation of groups acquiring specialized trophic habits. In accord with this hypothesis, a previous study demonstrated consistently greater diversification in clades attacking higher plants, as contrasted to their predaceous or saprophagous sister groups. Faster diversification of phytophagous insects could represent radiation in an unsaturated adaptive zone or result from the population fragmentation and diversifying selection imposed by ecological specialization per se. The latter effect underlies the hypothesis that rapid diversification characterizes ''parasitic'' insects in a broad sense including most phytophages, contrasting with the classical view of parasitic specialization as an evolutionary ''dead end.'' To test these hypotheses, we catalogued the origins and effect on diversification of animal parasitism by insects. Of 15 carnivorous parasitic insect clades with estimated relationships, six were more diverse than their predaceous or saprophagous sister groups, and nine less diverse (Wilcoxon T = 28, P < .10). The parasitic lifestyle in the broad sense is by itself unlikely to be a dominant explanation of variable insect diversification rate, while the hypothesis that parasitism in the strict sense is an evolutionary dead end remains plausible. Carnivorous parasitism and phytophagy have significantly different effects on diversification. We found no evidence for ascribing either this difference or the heterogeneity of rates among carnivorous parasite clades to clade age, mode of parasitism, diversity of host clade, or host specificity. Greater diversification by phytophages than by other trophic levels might reflect simply greater average abundance of the resource used by primary consumers.

Wiegmann, B. M., C. Mitter, and B. D. Farrell. 1993. Diversification of carnivorous parasitic insects: Extraordinary radiation or specialized dead end? American Naturalist 142:737-754. pdf

The spectacular diversity of insects has often been attributed to accelerated radiation of groups acquiring specialized trophic habits. In accord with this hypothesis, a previous study demonstrated consistently greater diversification in clades attacking higher plants, as contrasted to their predaceous or saprophagous sister groups. Faster diversification of phytophagous insects could represent radiation in an unsaturated adaptive zone or result from the population fragmentation and diversifying selection imposed by ecological specialization per se. The latter effect underlies the hypothesis that rapid diversification characterizes "parasitic" insects in a broad sense including most phytophages, contrasting with the classical view of parasitic specialization as an evolutionary "dead end." To test these hypotheses, we catalogued the origins and effect on diversification of animal parasitism by insects. Of 15 carnivorous parasitic insect clades with estimated relationships, six were more diverse than their predaceous or saprophagous sister groups, and nine less diverse (Wilcoxon T = 28, P lt .10). The parasitic lifestyle in the broad sense is by itself unlikely to be a dominant explanation of variable insect diversification rate, while the hypothesis that parasitism in the strict sense is an evolutionary dead end remains plausible. Carnivorous parasitism and phytophagy have significantly different effects on diversification. We found no evidence for ascribing either this difference or the heterogeneity of rates among carnivorous parasite clades to clade age, mode of parasitism, diversity of host clade, or host specificity. Greater diversification by phytophages than by other trophic levels might reflect simply greater average abundance of the resource used by primary consumers.

Mitter, C., B. D. Farrell, and D. J. Futuyma. 1991. Phylogenetic studies of insect-plant interactions: Insights into the genesis of diversity. Trends in Ecology and Evolution 6:290-293.

Phylogenetic analyses (and related historical evidence) can be used to test hypotheses about the opportunity for coevolution among plants and insect herbivores, the role of plant chemistry in mediating host shifts, the reality of coevolutionary 'arms races', and the role of novel defensive or counterdefensive characteristics in enhancing rates of diversification. Recent analyses provide evidence on each of these hypotheses. The strong phylogenetic component in many insect-plant associations suggests that host shifts by insects are often strongly constrained, that insect diets may not be 'optimal', and that the trophic structure and species diversity of local communities strongly reflect evolutionary history.

Farrell, B. D., D. E. Dussourd, and C. Mitter. 1991. Escalation of plant defenses: Do latex and resin canals spur plant diversification? American Naturalist 138:881-900. pdf

Ehrlich and Raven's 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). Explantations for this result, other than selective advantage conferred by secretory canals, are examined and provisionally rejected.

Farrell, B., and C. Mitter. 1990. Macroevolution of insect-plant antagonisms. American Journal of Botany 77:S174.

Herbivore evolution may be influenced by hostplant affiliation. Paleontological evidence suggests that many associated insect and plant groups are of comparable ages. In most insect groups for which there are cladograms, less than 20% of speciation events are accompanied by shift in host family association. Congruence of plant and herbivore phylogenies is rare, but demonstrable for one monophagus leaf beetle genus showing intricate dependence on the host. Partial concordance between phylogenies of other ecological associates may also reflect parallel diversification. Plant evolution may also sometimes be driven by herbivores. Sister group comparisons show that plant clades bearing latex or resin canal systems, which have arisen many times and for which experimental evidence stringly supports a defensive function, have significanlty enhanced diversification rates. Latex and resin-canal bearing plant species are also shown to be unusually abundant in some neotropical forests, suggesting that search for diversifying mechanisms may be warranted. The evolution of host-affiliation may generate global patterns of diversity. In a forest canopy in amazonian Peru, the diversity and distribution of herbivorous leaf-beetles reflect affiliation with particular hostplants while those of predaceous rove beetles are related to the volume of canopy foliage. Gradients in leaf-beetle distribtuion and diversity across latitudes and in the fossil record also reflect the role of host-specialization in the diversification of these herbivores. Other latitudinal gradients in diversity or distribution may be explained by processes more genreal that can be attributed to tropical of temperate biomass.

Farrell, B. D., and C. Mitter. 1990. Phylogenesis of insect-plant interactions: Have Phyllobrotica leaf beetles (Chrysomelidae) and the Lamiales diversified in parallel? Evolution 44:1389-1403. pdf


The relative importance of conservative versus locally adapted traits for species interactions is an increasingly common theme in evolutionary ecology. Obligate interactions such as those between parasites and hosts often exhibit such strong phylogenetic conservatism that current associations may reflect diversification in parallel. Parallel phylogenesis, documented for animal parasites, has been doubted for insect/plant interactions, but phylogenetic studies of highly specific insect/plant associations are very few. A comparison of phylogeny estimates for the strictly monophagous Phyllobrotica leaf beetles and their lamialean hostplants shows nearly complete concordance, strongly supporting the hypothesis of parallel diversification. The cladogram concordance is significant or nearly so (consensus index values equalling or exceeding the critical value) under randomization distributions based on Adams (though not Nelson) consensus trees. The one clear exception shows unusual natural history, suggesting an isolated host transfer. Insect distributions and plant fossil ages are consistent with a mid-Tertiary age for both clades, further disfavoring the alternative hypothesis of entirely subsequent evolution. The dependence of both larval and adult beetles on the hostplants, larval endophagy, and possible dependence of beetles on toxic host compounds for defense against predators are suggested to underlie the evolutionary persistence of this interaction. Current host use in these beetles appears to reflect primarily the phylogeny of the interaction, strengthening the thesis that history can play a major role in structuring insect/plant relationships.

Mitter, C., B. D. Farrell, and B. M. Wiegmann. 1988. The phylogenetic study of adaptive zones: Has phytophagy promoted insect diversification? American Naturalist 132:107-128. pdf

The relative importance of conservative versus locally adapted traits for species interactions is an increasingly common theme in evolutionary ecology. Obligate interactions such as those between parasites and hosts often exhibit such strong phylogenetic conservatism that current associations may reflect diversification in parallel. Parallel phylogenesis, documented for animal parasites, has been doubted for insect/plant interactions, but phylogenetic studies of highly specific insect/plant associations are very few.

A comparison of phylogeny estimates for the strictly monophagous Phyliobrotica leaf beetles and their lamialean hostplants shows nearly complete concordance, strongly supporting the hypothesis of parallel diversification. The cladogram concordance is significant or nearly so (consensus index values equalling or exceeding the critical value) under randomization distributions based on Adams (though not Nelson) consensus trees. The one clear exception shows unusual natural history, suggesting an isolated host transfer. Insect distributions and plant fossil ages are consistent with a mid-Tertiary age for both clades, funher disfavoring the alternative hypothesis of entirely subsequent evolution. The dependenceof both Larval and adult beetles on the hostplants, larval endophagy, and possible dependence of beetles on toxic host compounds for defense against predators are suggested to underlie the evolutionary persistence of this interaction. Current host use in these beetles appears to reflect primarily the phylogeny of the interaction, strengthenrng the thesis that history can play a major role in structuring insecuplant relationships.