Inordinate Fondness Research Articles

My Inordinate Fondness for Beetles and Other Musings

My Inordinate Fondness for Beetles and Other Musings

An inordinate fondness for inconspicuous brown frogs: integration of phylogenomics, archival DNA analysis, morphology, and bioacoustics yields 24 new taxa in the subgenus Brygoomantis (genus Mantidactylus) from Madagascar

Malagasy frogs of the subgenus Brygoomantis in the mantellid frog genus Mantidactylus currently comprise 14 described species of mostly brown, riparian frogs. Data from DNA barcoding suggested that the diversity of this subgenus is dramatically underestimated by current taxonomy. We here provide a comprehensive revision of this subgenus. We use hybrid-enrichment based DNA barcode fishing to obtain mitochondrial DNA fragments from the name-bearing type material of 16 of the 20 available names for members of this subgenus, and integrate these into a genetic dataset consisting of 1305 individuals sampled across Madagascar. By thus assigning the nomina to genetic lineages, we can confidently establish synonyms, revalidate old names, and describe the remaining diversity. We take an integrative approach to our descriptions, drawing together genetics, morphometrics and morphology, and bioacoustics for assignment. We also provide a robust phylogenomic hypothesis for the subgenus, based on 12,818 nuclear-encoded markers (almost 10 million base pairs) for 58 representative samples, sequenced using a hybrid-enrichment bait set for amphibians. Those data suggest a division of the subgenus into eight major clades and show that morphological species complexes are often paraphyletic or polyphyletic. Lectotypes are designated for Rana betsileana Boulenger, 1882; Rana biporus Boulenger, 1889; Rana curta Boulenger, 1882; Mantidactylus ambohimitombi Boulenger, 1918; Mantidactylus tripunctatus Angel, 1930; and Rana inaudax Peracca, 1893. For several other nomina, previous authors had considered a certain syntype as holotype; this has been seen as lectotype designation by implication, which, however, is ambiguous according to the provisions of the International Code of Zoological Nomenclature. Hence, we validate a previous lectotype designation by implication for Limnodytes ulcerosus Boettger, 1880 by explicitly designating the same individual as lectotype. In one other such case, that of Mantidactylus brauni Ahl, 1929, we deviate from previous authors and designate a different specimen as lectotype. We revalidate Rana inaudax Peracca, 1893 as Mantidactylus inaudax (Peracca, 1893) bona species, and Mantidactylus tripunctatus Angel, 1930 bona species. The identities of three further species (M. ambohimitombi, M. biporus, M. tricinctus) are largely redefined based on new genetic data. By designating the lectotype of Rana aluta (MZUT An725.1) as the neotype of Mantidactylus laevis Angel, 1929 we also stabilize the latter nomen (as junior synonym of M. alutus) whose original type material is lost. Based on DNA sequences of its lectotype, we consider Mantidactylus brauni Ahl, 1929 as junior synonym of M. ulcerosus (rather than M. biporus). We formally name 20 new species and four new subspecies: M. ambohimitombi marefo ssp. nov., M. ambohimitombi miloko ssp. nov., M. mahery sp. nov., M. steinfartzi sp. nov., M. incognitus sp. nov., M. jonasi sp. nov., M. katae sp. nov., M. kortei sp. nov., M. riparius sp. nov., M. fergusoni sp. nov., M. georgei sp. nov., M. jahnarum sp. nov., M. marintsoai sp. nov., M. grubenmanni sp. nov., M. gudrunae sp. nov., M. augustini sp. nov., M. bletzae sp. nov., M. brevirostris sp. nov., M. eulenbergeri sp. nov., M. glosi sp. nov., M. stelliger sp. nov., M. manerana sp. nov., M. manerana fotaka ssp. nov., and M. manerana antsanga ssp. nov. This leaves Mantidactylus subgenus Brygoomantis with 35 described species and six subspecies (including nominate subspecies). Based on our taxonomic revision, we discuss (i) the importance of definitive assignment of historical names via archival DNA analysis; (ii) the relevance of the subspecies category to name geographic variation within species; (iii) the value of molecular characters in formal species diagnoses in taxa with substantial individual variation of morphology; (iv) the use of phylogenomic approaches for taxonomy, by confirming that some morphologically similar taxa are not each other’s closest relatives, and in several cases belong to entirely different major subclades within Brygoomantis, thus facilitating lineage diagnosis; and (v) the need to interpret genetic distances in a probabilistic framework rather than using fixed thresholds, where higher distances confer a higher likelihood of genetic incompatibilities across the genome and thus completion of speciation.

Hutchinson’s tree

"There is a story, perhaps apocryphal, of the distinguished British biologist, J.B.S. Haldane, who found himself in the company of a group of theologians. On being asked what one could conclude as to the nature of the Creator from a study of his creation, Haldane is said to have answered “An inordinate fondness for beetles!”.

An inordinate fondness for species with intermediate dispersal abilities

J. B. S. Haldane is widely quoted to have quipped that the Creator, if one exists, has an inordinate fondness for beetles. Although Coleoptera may not be the most speciose order once Hymenopteran diversity is fully accounted for, as a whole the very clear differences in species diversity among taxa require an explanation. Here we use stochastic simulations to show that dispersal has eco‐evolutionary effects that predict taxa to become particularly species‐rich when dispersal is neither too low nor too high. Our model combines recent advances in understanding coexistence in niche space with previously verbally expressed ideas, where too low dispersal imposes biogeographic constraints that prevent a lineage from finding new areas to colonize (reducing opportunities for speciation), while too high dispersal impedes population divergence, leading to few but widely distributed species. We show that this logic holds for species richness and is robust to a variety of model assumptions, but peak diversification rate is instead predicted to increase with dispersal. Our work unifies findings of increasing and decreasing effects of dispersal rate on speciation, and explains why taxa with moderate dispersal abilities have the best prospects for high global species richness.

Inordinate Fondness Multiplied and Redistributed: the Number of Species on Earth and the New Pie of Life

AbstractThe number of species on Earth is one of the most fundamental numbers in science, but one that remains highly uncertain. Clearly, more species exist than the present number of formally described species (approximately 1.5 million), but projected species numbers differ dramatically among studies. Recent estimates range from about 2 million species to approximately 1 trillion, but most project around 11 million species or fewer. Numerous studies have focused on insects as a major component of overall richness, and many have excluded other groups, especially non-eukaryotes. Here, we re-estimate global biodiversity. We also estimate the relative richness of the major clades of living organisms, summarized as a “Pie of Life.” Unlike many previous estimates, we incorporate morphologically cryptic arthropod species from molecular-based species delimitation. We also include numerous groups of organisms that have not been simultaneously included in previous estimates, especially those often associated with...

The call of the not-so-mild

![Graphic][1] Flies and many other insects show an inordinate fondness for feces. They oviposit there and occasionally visit animal excrement to dine. But it turns out that not all poop is created equal, and flies are rather discerning in their choice of fecal targets. While some piles of

Nature's inordinate fondness for metabolic enzymes: why metabolic enzyme loci are so frequently targets of selection

Metabolic enzyme loci were some of the first genes accessible for molecular evolution and ecology research. New technologies now make the whole genome, transcriptome or proteome readily accessible, allowing unbiased scans for loci exhibiting significant differences in allele frequency or expression level and associated with phenotypes and/or responses to natural selection. With surprising frequency and in many cases in proportions greater than chance relative to other genes, glycolysis and TCA cycle enzyme loci appear among the genes with significant associations in these studies. Hence, there is an ongoing need to understand the basis for fitness effects of metabolic enzyme polymorphisms. Allele-specific effects on the binding affinity and catalytic rate of individual enzymes are well known, but often of uncertain significance because metabolic control theory and in vivo studies indicate that many individual metabolic enzymes do not affect pathway flux rate. I review research, so far little used in evolutionary biology, showing that metabolic enzyme substrates affect signalling pathways that regulate cell and organismal biology, and that these enzymes have moonlighting functions. To date there is little knowledge of how alleles in natural populations affect these phenotypes. I discuss an example in which alleles of a TCA enzyme locus associate with differences in a signalling pathway and development, organismal performance, and ecological dynamics. Ultimately, understanding how metabolic enzyme polymorphisms map to phenotypes and fitness remains a compelling and ongoing need for gaining robust knowledge of ecological and evolutionary processes.

Another inordinate fondness†: diversity of the tanaidacean fauna of Australia, with description of three new taxa

The shallow-water tanaidacean fauna of the Bass Strait has been the subject of recent intensive studies. The present paper extends this work into the deeper waters of the region, describing two new species and one new genus. The new species of the genus Paradoxapseudes has a combination of three maxillule palp setae, no plumose setae on the basis of pereopod 1 nor proximal serration on the antennal peduncle. The second species represents a new genus of the family Anarthruridae, having six marginal setae on the third maxilliped palp article and spines on the merus and carpus of the anterior pereopods. The high diversity of Tanaidacea in Australian waters is discussed. In particular, we conclude that Australian coasts suffer a diversity of immigration routes, have sufficient marine longevity, and afford such a diversity of available niches to have allowed multiple colonization and subsequent allopatric speciation of Tanaidacea. http://www.zoobank.org/urn:lsid:zoobank.org:pub:EE309A5A-E06D-416F-95BD-4C8D0D2BEB97

An Inordinate Fondness of Rarity

An Inordinate Fondness of Rarity

An inordinate fondness for Fusarium: Phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus Euwallacea on avocado and other plant hosts

Ambrosia beetle fungiculture represents one of the most ecologically and evolutionarily successful symbioses, as evidenced by the 11 independent origins and 3500 species of ambrosia beetles. Here we document the evolution of a clade within Fusarium associated with ambrosia beetles in the genus Euwallacea (Coleoptera: Scolytinae). Ambrosia Fusarium Clade (AFC) symbionts are unusual in that some are plant pathogens that cause significant damage in naïve natural and cultivated ecosystems, and currently threaten avocado production in the United States, Israel and Australia. Most AFC fusaria produce unusual clavate macroconidia that serve as a putative food source for their insect mutualists. AFC symbionts were abundant in the heads of four Euwallacea spp., which suggests that they are transported within and from the natal gallery in mandibular mycangia. In a four-locus phylogenetic analysis, the AFC was resolved in a strongly supported monophyletic group within the previously described Clade 3 of the Fusarium solani species complex (FSSC). Divergence-time estimates place the origin of the AFC in the early Miocene ∼21.2Mya, which coincides with the hypothesized adaptive radiation of the Xyleborini. Two strongly supported clades within the AFC (Clades A and B) were identified that include nine species lineages associated with ambrosia beetles, eight with Euwallacea spp. and one reportedly with Xyleborus ferrugineus, and two lineages with no known beetle association. More derived lineages within the AFC showed fixation of the clavate (club-shaped) macroconidial trait, while basal lineages showed a mix of clavate and more typical fusiform macroconidia. AFC lineages consisted mostly of genetically identical individuals associated with specific insect hosts in defined geographic locations, with at least three interspecific hybridization events inferred based on discordant placement in individual gene genealogies and detection of recombinant loci. Overall, these data are consistent with a strong evolutionary trend toward obligate symbiosis coupled with secondary contact and interspecific hybridization.

An “Inordinate Fondness for Transporters” Explained?

An often-asked question is, Why are there so many different transporters in a cell to take up a particular substrate? At least part of the answer comes from work on the possible competitive advantage of dual-transporter systems. In such systems, low-affinity transporters function when a nutrient is plentiful in the environment, and the abundance of high-affinity transporters is increased when that nutrient becomes scarce. A dual-transporter system enabled a long "preparation phase" to occur during which cells induce gene expression as they become increasingly starved. Surprisingly, the preparation phase is important not for growth under low-nutrient conditions but rather for fluctuating nutrient amounts as commonly occurs in nature. Thus, this creative study provides a previously unconsidered explanation for the abundance of dual-transporter systems in biology.

Towards a Temporal Framework for “Inordinate Fondness”: Reconstructing the Macroevolutionary History of Beetles (Coleoptera)

Abstract Most molecular phylogenetic studies of beetles (order Coleoptera) using 18S rDNA have recovered the suborders Adephaga and Polyphaga as sister groups, together sister to the suborders Myxophaga and Archostemata, with Archostemata alone or in combination with Myxophaga as the closest relative of all other beetles. Analyses of data from other genes have recovered alternative arrangements. Estimated subordinal divergence times based on analyses of DNA sequence data and fossil calibrations range from ∼ 285–266 million years ago (Ma), with most extant families estimated to have originated in the Jurassic. However, timing and patterns of ecological and taxonomic diversification remain uncertain for most beetle groups primarily due to limited gene and nucleotide sampling, missing data, and a corresponding lack of well-supported resolution. Consequently, the nature and degree to which events in earth's history (e.g., the diversification and rise of angiosperms to ecological dominance) have influenced the...

Genomics: An Inordinate Fondness for Beetles

Beetles are reckoned to make up about one quarter of animal species. Now, the first genome of a beetle--the red flour beetle Tribolium castaneum, a pest and developmental model system alike--has been sequenced.

D. Grimaldi & M. S. Engel 2005. Evolution of the Insects. xv + 755 pp. Cambridge, New York, Melbourne: Cambridge University Press. Price £45.00, US $75.00 (hard covers). ISBN 0 521 82149 5.

Like any subject biology has its worn-out metaphors. Scarcely less of a cliche than Dobzhansky’s dictum that nothing in biology makes sense except in the light of evolution, so Haldane’s quip that the Creator’s fructifying genius might seem odd given his inordinate fondness for beetles is long past its sell-by date (to compound the cliches). But if there was ever a case to be made that even within the beetles, let alone the insects, the variety of forms verges on the marvellous then this book will provide the gold-standard for years to come. Its most obvious advantage is the superb range of illustrations, from the golden tombs of amber to vivid …

An inordinate fondness for Mecopteriformia

What is the Largest animal taxon? The most famous answer to this question has been given by Haldane who coined the phrase that ‘the Creator has an inordinate fondness for beetles’. Although much cited, this statement has never been tested. Other experts have suggested other candidates for the largest animal taxon, all of which included the beetles as a subordinate group. I here outline a novel phylogenetic‐comparative method that can address the question in a testable way. The result of applying the algorithm to the Metazoa is astonishing: the largest animal taxon is neither beetles nor a taxon super‐ or subordinated to beetles, but the Mecopteriformia.

‘Inordinate Fondness’: A Threat to Beetles in South East Asia?

A recent report on trade in stag beetles and rhinoceros beetles in Japan highlights a number of issues of considerable importance for beetle conservation resulting from such trade over much of south east Asia. The popularity of these beetles has both positive and negative effects, and there is need for more effective control and monitoring of this trade to enhance positive values and reduce likely harm to species and habitats.

DONOGHUE, P. C. J. & SMITH, M. P. (eds) 2004. Telling the Evolutionary Time. Molecular Clocks and the Fossil Record. Systematics Association Publication no. 66. viii + 288 pp. Boca Raton, London, New York, Washington D.C.: CRC Press (Taylor & Francis), for the Systematics Association. Price £72.99 (hard covers). ISBN 0 415 27524 5

J. B. S. Haldane, famous for his quip about the Creator’s inordinate fondness for beetles, is also well known for his reply as to whether anything might make him abandon his belief in evolution. The response was to the effect that a rabbit found fossilized in Ordovician strata would shake his faith to the core. Haldane’s reply was hardly surprising; we do not find Ordovician rabbits any more than we do Devonian tulips or Cambrian dinosaurs. To the first approximation, the history of life shows an overall order that investigations of the fossil record continuously refine, but these days very seldom overthrow. In recent years, however, and perhaps as a distant echo of the corrosive relativism of the Kuhnian world picture of paradigm shifts, the old securities seem to have been eroded. One topical instance is the renewed questioning of whether the effect of the available sediment in a given geological interval, as well as other factors, such as Raup’s ‘Pull of the Recent’, do not conspire to distort completely any original diversity trends. Of equal, if not greater, importance, is the rather extraordinary fact that with few exceptions the estimated times of divergence that are based on molecular ‘clocks’ significantly exceed the palaeontological data points of first appearances. The implications are as obvious as they are intriguing. Could it be that the …

Book Reviews

Book Reviews

A macroevolutionary fondness for Neoptera

J.B.S. Haldane is famously supposed to have remarked that the Creator had an inordinate fondness for beetles. In evolutionary biologists’ minds, beetles have been basking in the warm glow of God's favour ever since: but are they really the chosen ones? Peter Mayhew [1] has now addressed this issue using data on species richness, taxon age and phylogenetic relatedness of hexapods (the Entognatha, e.g. Collembola, plus the insects) and concludes that the Creator's fondness had wider taxonomic bounds.

Studies in Quaternary Entomology—an Inordinate Fondness for Insects

Studies in Quaternary Entomology—an Inordinate Fondness for Insects