From Best to Worst?: (Another) Reevaluation of mtDNA as a Molecular Marker

Once the golden child of molecular phylogenetic and phylogeographic analyses, mtDNA has taken a beating over the past five years. There is a bit of irony to this backlash: many of the features that were once thought to make mtDNA a particularly desirable marker (e.g., lack of recombination, maternal inheritance, low effective population size), are now being cited as contributors to its worst problems, introgression and discordance with species boundaries being two of the most serious. Although discussion of these problems isn't hard to come by (1, 2), Galtier et al.'s recent review in Molecular Ecology is a particularly insightful contribution.

Galtier et al. use a myth-busting review of the recent literature to investigate three widespread claims about mtDNA: strict clonal evolution (lack of recombination), selective neutrality, and constant mutation rate. Galtier et al.'s take on clonal evolution provides one of few encouraging findings: although numerous recent studies recover within-species homoplasy that may be interpreted as evidence for recombination, Galtier et al. suggest that this apparent homoplasy may also result from mutational hot-spots.

The suggestion that mtDNA is selectively neutral is an assumption that is most in need of a good thrashing, and Galtier et al. are happy to oblige. After a brief discussion of the powerful evidence for selection and selective sweeps, Galtier et al. provide a nice discussion of both the possible causes for these phenomena and their far-reaching implications. The last paragraph of this section sums things up rather nicely: "Whatever the underlying causes of the patterns [of selection] observed, these studies demonstrate that the withinspecies level of mtDNA diversity per se is not a good marker of population size and species health, as observed both at the metazoa and mammalian levels. Nonequilibrium processes apparently dominate. The classical interpretation of genetic diversity as the product of mutation rate by population size, as expected at mutation-drift equilibrium, is strongly questionable as far as mtDNA data are concerned."

Finally, Galtier et al. provide evidence - primarily from Nabholz et al.'s (2008) recent reviews (1, 2) - that rates of mtDNA evolution are widely variable, both within and among taxa. They conclude suggesting: "The molecular clock, therefore, is certainly not a tenable assumption as far as mtDNA is concerned. Nonclock- like evolution is common, and the departure from homogeneous rates can be very strong."

Conspicuously absent from Galtier et al.'s review is a discussion of the feature of mtDNA that has most challenged recent phylogenetic and phylogeographic studies: introgression. Perhaps Galtier et al. viewed this as a topic already addressed by other reviews, but the mechanisms underling mtDNA introgression remain poorly understood and this topic too would have benefitted from Galtier et al.'s insight.

At the end of the day, Galtier et al. take a rather dire view of mtDNA as a molecular marker, suggesting that its primary value is in its cheapness. Although I have a bit more charitable view, I certaintly hope that Galtier et al.'s review will succeed in opening more eyes to the diversity of problems confronting interpretation of mtDNA.

GALTIER, N., NABHOLZ, B., GLÉMIN, S., & HURST, G. (2009). Mitochondrial DNA as a marker of molecular diversity: a reappraisal Molecular Ecology, 18 (22), 4541-4550 DOI: 10.1111/j.1365-294X.2009.04380.x

New Applications of Population Genetic Methods to Studies of Language Evolution

A recent study in PLoS biology nicely illustrates how modern studies of language evolution and geographic variation are taking advantage of modern population genetic and phylogenetic methods. Although the use of phylogenetic methods in quantititive comparative linguisitics isn't new, this new study is, to my knowledge, the first to use the Bayesian clustering algorithms that are all the rage in population genetics. This study uses these methods to investigate the extraordinarily diverse languages of Sahul (an ancient continent formed from present day Australia, New Guinea and surrounding islands). Previous attempts to infer the history of these languages have been complicated by two problems that will be familiar to any phylogeneticist. The first problem involves identification of homologies - or, in the jargon of a quantitative comparative linguist "phonological and semantic drift [which] make it impossible to identify lexical cognate characters." Another challenge stems from admixture, which may result from the fact that many Sahul languages have been in "long term and intensive contact," . By applying the program Structure to 160 "abstract structural features" quantified for 121 Sahul languages, Reesink et al. are able to recover 10 "ancestral language populations." Many of the clusters recovered by Structure correspond with previously diagnosed language groupings, and the overall patterns of hierarchical clustering suggest plausible historical scenarios. The authors also suggest that, in spite of ample opportunity for interchange, many languages show "negligible amounts of admixture."

Reesink, G., Singer, R., & Dunn, M. (2009). Explaining the Linguistic Diversity of Sahul Using Population Models PLoS Biology, 7 (11) DOI: 10.1371/journal.pbio.1000241

More From Inside (and Outside) the Fringe

A recent post to this blog was regarding the article in PNAS positing a hybrid origin for the larval stage of lepidopterans (the insect order containing moths and butterflies). More specifically, Williamson (2009) proposed that modern lepidopterans, with their highly complex larval life stage and metamorphosis, acquired it not by the traditional neo-Darwinian means of descent with modification, but instead by hybridogenesis with adult onychophorans – the latter being an ancient, distantly related group thought to be the sister group to Arthropoda (the animal phylum of lepidopterans and all other insects, as well as groups as varied as crabs, millipedes, and barnacles).

Considerable negative attention has been directed towards Williamson’s kooky idea since it was published – and even more to the fact that it was published in one of the more prestigious journals of our field – and still more to the (possibly unscrupulous) manner that the article was handled by the communicating National Academy member, Lynn Margulis. Much of this rapid-fire negative attention came from the blogosphere, most notably from Jerry Coyne who dubbed the article the “worst paper of the year” on his popular “Why Evolution is True” blog.

A more formal scientific response was sure to follow. First, Gonzalo Giribet of Harvard responded with a short letter to PNAS entitled “On velvet worms and caterpillars: Science, fiction, or science fiction?” in which he points out that, in making his claims to the hybrid origin of lepidopteran larvae, Williamson has gratuitously overlooked a large body of phylogenetic evidence showing that onycophorans are the sister group to arthropods, and not closely related to either larval or adult lepidopterans.

More recently, Michael Hart and Richard Grosberg went farther, publishing a very thorough and deliberate rebuttal to Williamson (2009). In a "Mythbusters" style article uncreatively (but fittingly) entitled “Caterpillars did not evolve from onychophorans by hybridogenesis” (emphasis mine) they systematically review virtually all of the predictions of Williamson’s hypothesis. . . and just as systematically reject them! For instance, Williamson predicts that under his hybridogenesis theory holometabolous (metamorphic) insects will have larger genomes than non-metamorphic insects. Hart and Grosberg point out that C-value (whole genome size) information exists for a wide range of insect species in metamorphic and non-metamorphic groups. Analysis of these data has revealed that, in fact, species in holometabolous insect orders have genome sizes that are on average smaller (not larger) than non-metamorphic insects, although the ranges of genome size in both groups overlap broadly. Numerous other predictions from Williamson (2009) are similarly tested and rejected.

Since I originally blogged on this subject over two months ago several additional comments about the article, the “crackpot index” of the author, or the submission and review process at PNAS have appeared online (e.g., here, here, and here). Horrifyingly (but predictably) the “Institute of Creation Research” has even picked up on the controversy, labeling it as evidence for “deep disagreement” among evolutionary biologists (I’m loath to link to the article here, lest that in so doing I increase the page rank of the ICR website). My interpretation is to the contrary. Controversy abounds in our field, as it should in any vital, active area of science. However, rarely have I seen a group of evolutionary biologists as unified as they have been against this contrary theory and furthermore its questionable publication in a respected journal of our field!

Dechronization Showcased on Medpedia

Some of you may have noticed the little badge on the left side of our website for Medpedia. The Medpedia Project is the web-based platform that seeks to be a repository for all things health-related, with its goal of linking physicians, scientists, health-related agencies, consumers and others. This week they have added a new feature called "News and Analysis" that links to content from a few select blogs. Dechronization was chosen to be one of these showcased blogs, under the "Science and Research" category.

Dispatches from the 2009 North American Symposium on Bat Research

I just returned from the 2009 North American Symposium on Bat Research, held in - where else? - Portland, Oregon. I know I usually see myself as more of a herpetologist, but some recent work I've been doing on malaria parasites in bats prompted this westward trek to meet other bat biologists and return to my roots (my undergrad advisor, Roy Horst, was one of the founders of the society and my first grad project was on Trinidadian bats with Jerry Wilkinson). A few highlights from these meetings: Aaron Corcoran, a grad student at Wake Forest gave a nice paper describing some very cool experiments that show that tiger moths use "clicks" that they make to jam up the echolocation of big brown bats and avoid predation. That project was published in Science this summer. Sharlene Santana, a student at UMass Amherst demonstrated the spread of the Anthony "Biteforce" Herrel cult, by giving a talk about plasticity in bite force in frugivorous neotropical bats, an evolutionary trend that she suggests contributed to their notable diversification. I gave a talk in a special session on "Health and Disease" in bats and one of my (other) favorites in that session was by Daniel Streicker from the University of Georgia who gave some really nice estimates of rabies virus transmission between species of bats within a community using coalescent-based model approaches, showing that bats are more likely to infect phylogenetically related species, but at unequal rates. Elizabeth Clare, from Guelph, used DNA barcoding (duh - she's at Guelph!) of guano to generate some very intriguing data about resource partitioning in two (to eight - she had somewhat smaller datasets for another six) species of sympatric bats. And the last talk that I got to see before having to run off to catch a plane was by Robert Baker, of Texas Tech, who summarized three important types of speciation in bats - ecological, hybrid and adaptive radiations and gave examples of each. Baker, answering his own question, "Genetics, what have you done for bats lately?" suggested that the number of species of bats may soon increase by as much as 50% just due to better studies of molecular variation in cryptic and hybrid species. The North American Society of Bat Researchers is certainly all like a big family to each other and it was nice to crash their annual reunion.