Jack Sullivan

Performance-Based Selection of Likelihood Models for Phylogeny Estimation

Phylogenetic estimation has largely come to rely on explicitly model-based methods. This approach requires that a model be chosen and that that choice be justified. To date, justification has largely been accomplished through use of likelihood-ratio tests (LRTs) to assess the relative fit of a nested series of reversible models. While this approach certainly represents an important advance over arbitrary model selection, the best fit of a series of models may not always provide the most reliable phylogenetic estimates for finite real data sets, where all available models are surely incorrect. Here, we develop a novel approach to model selection, which is based on the Bayesian information criterion, but incorporates relative branch-length error as a performance measure in a decision theory (DT) framework. This DT method includes a penalty for overfitting, is applicable prior to running extensive analyses, and simultaneously compares all models being considered and thus does not rely on a series of pairwise comparisons of models to traverse model space. We evaluate this method by examining four real data sets and by using those data sets to define simulation conditions. In the real data sets, the DT method selects the same or simpler models than conventional LRTs. In order to lend generality to the simulations, codon-based models (with parameters estimated from the real data sets) were used to generate simulated data sets, which are therefore more complex than any of the models we evaluate. On average, the DT method selects models that are simpler than those chosen by conventional LRTs. Nevertheless, these simpler models provide estimates of branch lengths that are more accurate both in terms of relative error and absolute error than those derived using the more complex (yet still wrong) models chosen by conventional LRTs. This method is available in a program called DT-ModSel.

Balancing hydropower and biodiversity in the Amazon, Congo, and Mekong

Basin-scale planning is needed to minimize impacts in mega-diverse rivers The worlds most biodiverse river basins—the Amazon, Congo, and Mekong—are experiencing an unprecedented boom in construction of hydropower dams. These projects address important energy needs, but advocates often overestimate economic benefits and underestimate far-reaching effects on biodiversity and critically important fisheries. Powerful new analytical tools and high-resolution environmental data can clarify trade-offs between engineering and environmental goals and can enable governments and funding institutions to compare alternative sites for dam building. Current site-specific assessment protocols largely ignore cumulative impacts on hydrology and ecosystem services as ever more dams are constructed within a watershed (1). To achieve true sustainability, assessments of new projects must go beyond local impacts by accounting for synergies with existing dams, as well as land cover changes and likely climatic shifts (2, 3). We call for more sophisticated and holistic hydropower planning, including validation of technologies intended to mitigate environmental impacts. Should anything less be required when tampering with the worlds great river ecosystems?

INVESTIGATING THE EVOLUTIONARY HISTORY OF THE PACIFIC NORTHWEST MESIC FOREST ECOSYSTEM: HYPOTHESIS TESTING WITHIN A COMPARATIVE PHYLOGEOGRAPHIC FRAMEWORK

Abstract We examine the evolution of mesic forest ecosystems in the Pacific Northwest of North America using a statistical phylogeography approach in four animal and two plant lineages. Three a priori hypotheses, which explain the disjunction in the mesic forest ecosystem with either recent dispersal or ancient vicariance, are tested with phylogenetic and coalescent methods. We find strong support in three amphibian lineages (Ascaphus spp., and Dicampton spp., and Plethodon vandykei and P. idahoensis) for deep divergence between coastal and inland populations, as predicted by the ancient vicariance hypothesis. Unlike the amphibians, the disjunction in other Pacific Northwest lineages is likely due to recent dispersal along a northern route. Topological and population divergence tests support the northern dispersal hypothesis in the water vole (Microtus richardsoni) and northern dispersal has some support in both the dusky willow (Salix melanopsis) and whitebark pine (Pinus albicaulis). These analyses demonstrate that genetic data sampled from across an ecosystem can provide insight into the evolution of ecological communities and suggest that the advantages of a statistical phylogeographic approach are most pronounced in comparisons across multiple taxa in a particular ecosystem. Genetic patterns in organisms as diverse as willows and salamanders can be used to test general regional hypotheses, providing a consistent metric for comparison among members of an ecosystem with disparate life‐history traits.

Evolution of the Mitochondrial Cytochrome Oxidase II Gene in Collembola

Abstract. The sequence of the mitochondrial COII gene has been widely used to estimate phylogenetic relationships at different taxomonic levels across insects. We investigated the molecular evolution of the COII gene and its usefulness for reconstructing phylogenetic relationships within and among four collembolan families. The collembolan COII gene showed the lowest A + T content of all insects so far examined, confirming that the well-known A + T bias in insect mitochondrial genes tends to increase from the basal to apical orders. Fifty-seven percent of all nucleotide positions were variable and most of the third codon positions appeared free to vary. Values of genetic distance between congeneric species and between families were remarkably high; in some cases the latter were higher than divergence values between other orders of insects. The remarkably high divergence levels observed here provide evidence that collembolan taxa are quite old; divergence levels among collembolan families equaled or exceeded divergences among pterygote insect orders. Once the saturated third-codon positions (which violated stationarity of base frequencies) were removed, the COII sequences contained phylogenetic information, but the extent of that information was overestimated by parsimony methods relative to likelihood methods. In the phylogenetic analysis, consistent statistical support was obtained for the monophyly of all four genera examined, but relationships among genera/families were not well supported. Within the genus Orchesella, relationships were well resolved and agreed with allozyme data. Within the genus Isotomurus, although three pairs of populations were consistently identified, these appeared to have arisen in a burst of evolution from an earlier ancestor. Isotomurus italicus always appeared as basal and I. palustris appeared to harbor a cryptic species, corroborating allozyme data.

Comparative Phylogeography of Mesoamerican Highland Rodents: Concerted versus Independent Response to Past Climatic Fluctuations

The phylogeography of Sumichrast’s harvest mouse (Reithrodontomys sumichrasti) was examined through maximum‐likelihood and parsimony analyses of 1,130 bp of mitochondrial Cytochrome b sequence data from 43 individuals. The phylogeography of this Middle American highland forest‐dwelling species was compared to that previously published for the codistributed Aztec deer mouse complex (Peromyscus aztecus/Peromyscus hylocetes complex) in order to test competing hypotheses of concerted versus independent responses of codistributed forms to past climatic fluctuations. Qualitatively, there were strong similarities in the phylogeographic patterns of the two groups, yet there were also areas of incongruence. Likelihood‐ratio tests (Kishino‐Hasegawa‐Templeton and parametric bootstrap tests) indicated that this incongruence is significant and cannot be attributed simply to uncertainty in phylogenetic estimation, thereby falsifying the concerted‐response hypothesis. Conversely, tree‐reconciliation analysis of the area relationships inferred for each group separately indicated that there has been a significant history of covicariance between the two groups, falsifying the independent‐response hypothesis. It appears that codistributed taxa in the geologically complex highlands of Mesoamerica share more common biogeographical history than can be accounted for by the independent‐response hypothesis yet have not responded to past climatic fluctuations in the lock‐step fashion predicted by the concerted‐response hypothesis.

PHYLOGEOGRAPHY OF THE TAILED FROG (ASCAPHUS TRUEI): IMPLICATIONS FOR THE BIOGEOGRAPHY OF THE PACIFIC NORTHWEST

Tailed frogs are distributed in high‐gradient streams within the disjunct mesic forests of the Pacific North‐west and represent the basal lineage of the anurans. We sequenced 1530 nucleotides of the mitochondrial cytochrome b and NADH dehydrogenase subunit two genes from 23 populations and used parsimony, maximum‐likelihood, and nested‐clade analyses to estimate relationships among populations and infer evolutionary processes. We found two divergent haplotype clades corresponding with in land Rocky Mountain populations and coastal populations and separated by up to 0.133 substitutions per site. Within the coastal assemblage, haplotypes formed clades by mountain range with 0.010‐0.024 substitutions per site divergence among populations. Inland haplotypes exhibited minimal genetic structure, with the exception of 0.021 substitutions per site distance between populations from the East Fork of the South Fork of the Salmon River and all other inland haplotypes. The magnitude of divergence between inland and coastal populations, as well as the paleobotanical record, suggest isolation of these lineages occurred during the late Miocene to early Pliocene, probably in response to the rise of the Cascade Mountains. Genetic structure within coastal and inland populations is consistent with isolation in refugia during the late Pliocene and early Pleistocene. Closely related in land haplotypes reflect range expansion following glaciation. The depth of divergence between inland and coastal populations supports the persistence of mesic forests within the inland Pacific Northwest throughout the Pleistocene and is congruent with patterns found in several other mesic forest species. Based on mitochondrial divergence and previous allozyme and morphological data, we recommend recognition of inland populations as a distinct species, Ascaphus montanus.

Ancient hybridization and mitochondrial capture between two species of chipmunks

Models that posit speciation in the face of gene flow are replacing classical views that hybridization is rare between animal species. We use a multilocus approach to examine the history of hybridization and gene flow between two species of chipmunks (Tamias ruficaudus and T. amoenus). Previous studies have shown that these species occupy different ecological niches and have distinct genital bone morphologies, yet appear to be incompletely isolated reproductively in multiple areas of sympatry. We compared data from four sequenced nuclear loci and from seven microsatellite loci to published cytochrome b sequences. Interspecific gene flow was primarily restricted to introgression of the T. ruficaudus mitochondrial genome into a sympatric subspecies of T. amoenus, T. a. canicaudus, with the four sequenced nuclear loci showing little to no interspecific allele sharing. Microsatellite data were consistent with high levels of differentiation between the species and also showed no current gene flow between broadly sympatric populations of T. a. canicaudus and T. ruficaudus. Coalescent analyses date the mtDNA introgression event from the mid‐Pleistocene to late Pliocene. Overall, these data indicate that introgression has had a minimal impact on the nuclear genomes of T. amoenus and T. ruficaudus despite multiple independent hybridization events. Our findings challenge long‐standing assumptions on patterns of reproductive isolation in chipmunks and suggest that there may be other examples of hybridization among the 23 species of Tamias that occur in western North America.

AFLPs RESOLVE PHYLOGENY AND REVEAL MITOCHONDRIAL INTROGRESSION WITHIN A SPECIES FLOCK OF AFRICAN ELECTRIC FISH (MORMYROIDEA: TELEOSTEI)

Abstract Estimating species phylogeny from a single gene tree can be especially problematic for studies of species flocks in which diversification has been rapid. Here we compare a phylogenetic hypothesis derived from cytochrome b (cyt b) sequences with another based on amplified fragment length polymorphisms (AFLP) for 60 specimens of a monophyletic riverine species flock of mormyrid electric fishes collected in Gabon, west-central Africa. We analyze the aligned cyt b sequences by Wagner parsimony and AFLP data generated from 10 primer combinations using neighbor-joining from a Nei-Li distance matrix, Wagner parsimony, and Dollo parsimony. The different analysis methods yield AFLP tree topologies with few conflicting nodes. Recovered basal relationships in the group are similar between cyt b and AFLP analyses, but differ substantially at many of the more derived nodes. More of the clades recovered with the AFLP characters are consistent with the morphological characters used to designate operational taxonomic units in this group. These results support our hypothesis that the mitochondrial gene tree differs from the overall species phylogeny due at least in part to mitochondrial introgession among lineages. Mapping the two forms of electric organ found in this group onto the AFLP tree suggests that posteriorly innervated electrocytes with nonpenetrating stalks have independently evolved from anteriorly innervated, penetrating-stalk electrocytes at least three times.

Accounting for coalescent stochasticity in testing phylogeographical hypotheses: modelling Pleistocene population structure in the Idaho giant salamander Dicamptodon aterrimus

Several theoretical studies have demonstrated the importance of accounting for coalescent stochasticity in phylogeographical studies, however, there are few empirical examples that do so in the context of explicit hypothesis testing. Here, we provide an example from the Idaho giant salamander (Dicamptodon aterrimus) using 118 mtDNA sequences, nearly 2 kb in length. This species is endemic to mesic forests in northern and central Idaho, and several a priori hypotheses have been erected based both on palaeoclimatic grounds and from phylogeographical studies of codistributed amphibians. Phylogenetic analysis of the D. aterrimus data suggests an expansion from a single refugium south of the Salmon River, whereas the inference from nested clade analysis is one of expansion from a single refugium in the Clearwater drainage. Explicit testing of these hypotheses, using geographically structured coalescent simulations to erect null distributions, indicates we can reject expansion from the Clearwater drainage (pCLW = 0.089), but not expansion from the South Fork of the Salmon drainage (pSAL = 0.329). Furthermore, data from codistributed amphibians suggest that there may have been two refugia, and an amova shows that most of the molecular variance partitioned between the Clearwater and the Salmon drainages (54.40%; P < 0.001) and within drainages (43.61%; P < 0.001). As a result, we also tested three a priori hypotheses which predicted that both the Clearwater and Salmon drainages functioned as refugia during the late Pleistocene; we could reject (PCORD = 0.019) divergence dates during the Cordilleran glacial maxima [c. 20 000 years before present (ybp)], during the Sangamon interglacial (c. 35 000 ybp; pSANG = 0.032), as well as pre‐Pleistocene divergence (c. 1.7 Ma; ppP < 0.001). Mismatch distributions and Tajimas D within the individual drainages provide further support to recent population expansion. This work demonstrates coalescent stochasticity is an important phenomenon to consider in testing phylogeographical hypotheses, and suggests that analytical methods which fail to sufficiently quantify this uncertainty can lead to false confidence in the conclusions drawn from these methods.

Sexual signal evolution outpaces ecological divergence during electric fish species radiation.

Natural selection arising from resource competition and environmental heterogeneity can drive adaptive radiation. Ecological opportunity facilitates this process, resulting in rapid divergence of ecological traits in many celebrated radiations. In other cases, sexual selection is thought to fuel divergence in mating signals ahead of ecological divergence. Comparing divergence rates between naturally and sexually selected traits can offer insights into processes underlying species radiations, but to date such comparisons have been largely qualitative. Here, we quantitatively compare divergence rates for four traits in African mormyrid fishes, which use an electrical communication system with few extrinsic constraints on divergence. We demonstrate rapid signal evolution in the Paramormyrops species flock compared to divergence in morphology, size, and trophic ecology. This disparity in the tempo of trait evolution suggests that sexual selection is an important early driver of species radiation in these mormyrids. We also found slight divergence in ecological traits among closely related species, consistent with a supporting role for natural selection in Paramormyrops diversification. Our results highlight the potential for sexual selection to drive explosive signal divergence when innovations in communication open new opportunities in signal space, suggesting that opportunity can catalyze species radiations through sexual selection, as well as natural selection.