Jimmy A. McGuire

Coalescent-based species delimitation in an integrative taxonomy

The statistical rigor of species delimitation has increased dramatically over the past decade. Coalescent theory provides powerful models for population genetic inference, and is now increasingly important in phylogenetics and speciation research. By applying probabilistic models, coalescent-based species delimitation provides clear and objective testing of alternative hypotheses of evolutionary independence. As acquisition of multilocus data becomes increasingly automated, coalescent-based species delimitation will improve the discovery, resolution, consistency, and stability of the taxonomy of species. Along with other tools and data types, coalescent-based species delimitation will play an important role in an integrative taxonomy that emphasizes the identification of species limits and the processes that have promoted lineage diversification.

Genome 10K: A Proposal to Obtain Whole-Genome Sequence for 10 000 Vertebrate Species

The human genome project has been recently complemented by whole-genome assessment sequence of 32 mammals and 24 nonmammalian vertebrate species suitable for comparative genomic analyses. Here we anticipate a precipitous drop in costs and increase in sequencing efficiency, with concomitant development of improved annotation technology and, therefore, propose to create a collection of tissue and DNA specimens for 10,000 vertebrate species specifically designated for whole-genome sequencing in the very near future. For this purpose, we, the Genome 10K Community of Scientists (G10KCOS), will assemble and allocate a biospecimen collection of some 16,203 representative vertebrate species spanning evolutionary diversity across living mammals, birds, nonavian reptiles, amphibians, and fishes (ca. 60,000 living species). In this proposal, we present precise counts for these 16,203 individual species with specimens presently tagged and stipulated for DNA sequencing by the G10KCOS. DNA sequencing has ushered in a new era of investigation in the biological sciences, allowing us to embark for the first time on a truly comprehensive study of vertebrate evolution, the results of which will touch nearly every aspect of vertebrate biological enquiry.

Increased Taxon Sampling Is Advantageous for Phylogenetic Inference

Until recently, it was believed that complex phylogenies might be extremely difficult to reconstruct due to the phenomenal rate of increase in the number of possible phylogenies as the number of taxa increases. However, Hillis (1996) showed through simulation that, for at least one complex phylogeny of angiosperms with 228 taxa, reconstruction was far more accurate than expected, even with relatively modest amounts of DNA sequence data. This led to a flurry of papers on the subject of taxon sampling and phylogenetic reconstruction, with focus quickly shifting from the question of whether complex phylogenies can be reconstructed to whether and how much an existing phylogeny can be improved through increased taxon sampling (Hillis, 1998; Kim, 1998; Poe, 1998; Poe and Swofford, 1999; Pollock and Bruno, 2000; Rannala et al., 1998; Yang, 1998). Although a statistician might intuitively believe that it is generally better (or at least no worse) to increase the amount of data to resolve a question in statistical inference, the benefits of taxon addition for phylogenetic inference remain controversial. Some researchers have argued that taxon addition can decrease accuracy (Kim, 1996,1998), while others believe that increased sampling improves accuracy (Graybeal, 1998; Hillis, 1996, 1998; Murphy et al., 2001; Poe, 1998; Pollock and Bruno, 2000; Pollock et al., 2000; Soltis et al., 1999). The reasons that different papers come to apparently contradictory conclusions deserve careful consideration. An often cited factor affecting the benefits of taxon addition is the phenomenon of long-branch attraction (LBA). Some phylogenetic methods have a bias toward preferential clustering of long branches, leading to erroneous results when those long branches do not actually represent a monophyletic assemblage (Felsenstein, 1978; Hendy and Penny, 1989). This phenomenon has been cited in favor of increased taxon sampling, since sampling can be designed to break up long branches (Hillis, 1998). However, increased sampling has also been implicated as a potential cause of LBA because addition of a new long branch may wrongly attract a pre-existing long branch that had previously been inferred correctly (Poe and Swofford, 1999; Rannala et al., 1998). LBA may also explain some simulations that have found problems in phylogeny estimation when sampling outside the taxonomic group of interest (but see Pollock and Bruno [2000] for an alternative explanation). Outside sampling in these simulations tended to add long branches, which tended to attract the longest unbroken branch in the group of interest (Hillis, 1998; Rannala et al., 1998). The degree to which LBA is a problem depends greatly on the method of analysis, and LBA is much less of a problem for maximum likelihood (ML) than for parsimony or distance methods (Bruno and Halpern, 1999). A recent paper on the subject of taxon addition (Rosenberg and Kumar, 2001) concludes that increased taxon sampling is of little benefit to phylogenetic inference when compared to increasing sequence length. We disagree with their interpretation and believe that their data support the importance of increased taxon sampling. In addition, some of their data were simulated under extreme conditions (i.e., substitution rates that were very high or low, or sequences that were unreasonably short). Large error values and nonlinear relationships at these extremes make it difficult to interpret effects for the majority of the range, and averaging across the entire range is inappropriate. Moreover, we do not believe that Rosenberg and Kumar (2001) used the most appropriate metric to measure the relative effect of taxon addition. Our reanalysis of their simulated data indicates that increased taxon sampling is highly beneficial for phylogenetic inference.

Is sparse taxon sampling a problem for phylogenetic inference

Rosenberg and Kumar (2001) addressed the importance of taxon sampling in phylogenetic analysis and concluded that phylogenetic error is “largely independent of taxon sample size” (2001:10756) and that their “results do not provide evidence in favor of adding taxa to problematic phylogenies” (2001:10756). In response to these conclusions, Zwickl and Hillis (2002) and Pollock et al. (2002) conducted additional simulations and reanalyzed the data presented by Rosenberg and Kumar (2001). Zwickl and Hillis and Pollock et al. showed that these conclusions of Rosenberg and Kumar could not be supported either by analyses of their original data or by new simulations that corrected a number of deficiencies in Rosenberg and Kumar’s original experimental design. Both Zwickl and Hillis and Pollock et al. found that increased taxon sampling resulted in greatly reduced phylogenetic estimation error, and Pollock et al. showed that the benefits of increased taxon sampling were similar to adding an equivalent amount of sequence length for the same taxa (in the ranges simulated by Rosenberg and Kumar). In their response, Rosenberg and Kumar (2002) focused on a slightly different conclusion from that in their original paper, which was that “longer sequences, rather than extensive sampling, will better improve the accuracy of phylogenetic inference” (2001:10751). In 2001, Rosenberg and Kumar argued that the beneficial effect of increasing taxa was 10-fold lower than the beneficial effect of increasing sequence length and that the effects of increased taxon sampling for the same genes were negligible (“largely independently” of phylogenetic error). Rosenberg and Kumar (2002) have now concluded that the beneficial effect of increasing taxon sample size is not small, but they suggested that the benefit comes simply from the overall increase in size of the data matrix (the total number of characters × taxa). Furthermore, they maintained that there is a greater benefit to increasing the total sequence length for few taxa than can be obtained by increasing taxon sampling for the same genes. Here, we discuss the two sets of conclusions reached by Rosenberg and Kumar (2001, 2002).

Phylogenetic Systematics and Biogeography of Hummingbirds: Bayesian and Maximum Likelihood Analyses of Partitioned Data and Selection of an Appropriate Partitioning Strategy

Hummingbirds are an important model system in avian biology, but to date the group has been the subject of remarkably few phylogenetic investigations. Here we present partitioned Bayesian and maximum likelihood phylogenetic analyses for 151 of approximately 330 species of hummingbirds and 12 outgroup taxa based on two protein-coding mitochondrial genes (ND2 and ND4), flanking tRNAs, and two nuclear introns (AK1 and BFib). We analyzed these data under several partitioning strategies ranging between unpartitioned and a maximum of nine partitions. In order to select a statistically justified partitioning strategy following partitioned Bayesian analysis, we considered four alternative criteria including Bayes factors, modified versions of the Akaike information criterion for small sample sizes (AIC(c)), Bayesian information criterion (BIC), and a decision-theoretic methodology (DT). Following partitioned maximum likelihood analyses, we selected a best-fitting strategy using hierarchical likelihood ratio tests (hLRTS), the conventional AICc, BIC, and DT, concluding that the most stringent criterion, the performance-based DT, was the most appropriate methodology for selecting amongst partitioning strategies. In the context of our well-resolved and well-supported phylogenetic estimate, we consider the historical biogeography of hummingbirds using ancestral state reconstructions of (1) primary geographic region of occurrence (i.e., South America, Central America, North America, Greater Antilles, Lesser Antilles), (2) Andean or non-Andean geographic distribution, and (3) minimum elevational occurrence. These analyses indicate that the basal hummingbird assemblages originated in the lowlands of South America, that most of the principle clades of hummingbirds (all but Mountain Gems and possibly Bees) originated on this continent, and that there have been many (at least 30) independent invasions of other primary landmasses, especially Central America.

Phylogenetic structure in tropical hummingbird communities

How biotic interactions, current and historical environment, and biogeographic barriers determine community structure is a fundamental question in ecology and evolution, especially in diverse tropical regions. To evaluate patterns of local and regional diversity, we quantified the phylogenetic composition of 189 hummingbird communities in Ecuador. We assessed how species and phylogenetic composition changed along environmental gradients and across biogeographic barriers. We show that humid, low-elevation communities are phylogenetically overdispersed (coexistence of distant relatives), a pattern that is consistent with the idea that competition influences the local composition of hummingbirds. At higher elevations communities are phylogenetically clustered (coexistence of close relatives), consistent with the expectation of environmental filtering, which may result from the challenge of sustaining an expensive means of locomotion at high elevations. We found that communities in the lowlands on opposite sides of the Andes tend to be phylogenetically similar despite their large differences in species composition, a pattern implicating the Andes as an important dispersal barrier. In contrast, along the steep environmental gradient between the lowlands and the Andes we found evidence that species turnover is comprised of relatively distantly related species. The integration of local and regional patterns of diversity across environmental gradients and biogeographic barriers provides insight into the potential underlying mechanisms that have shaped community composition and phylogenetic diversity in one of the most species-rich, complex regions of the world.

MITOCHONDRIAL INTROGRESSION AND INCOMPLETE LINEAGE SORTING THROUGH SPACE AND TIME: PHYLOGENETICS OF CROTAPHYTID LIZARDS

Abstract We investigate the roles of mitochondrial introgression and incomplete lineage sorting during the phylogenetic history of crotaphytid lizards. Our Bayesian phylogenetic estimate for Crotaphytidae is based on analysis of mitochondrial DNA sequence data for 408 individuals representing the 12 extant species of Crotaphytus and Gambelia. The mitochondrial phylogeny disagrees in several respects with a previously published morphological tree, as well as with conventional species designations, and we conclude that some of this disagreement stems from hybridization-mediated mitochondrial introgression, as well as from incomplete lineage sorting. Unidirectional introgression of Crotaphytus collaris (western collared lizard) mitochondria into C. reticulatus (reticulate collared lizard) populations in the Rio Grande Valley of Texas has resulted in the replacement of ancestral C. reticulatus mitochondria over approximately two-thirds of the total range of the species, a linear distance of ∼270 km. Introgression of C. collaris mitochondria into C. bicinctores (Great Basin collared lizard) populations in southwestern Arizona requires a more complex scenario because at least three temporally separated and superimposed introgression events appear to have occurred in this region. We propose an “introgression conveyor” model to explain this unique pattern of mitochondrial variation in this region. We show with ecological niche modeling that the predicted geographical ranges of C. collaris, C. bicinctores, and C. reticulatus during glacial maxima could have provided enhanced opportunities for past hybridization. Our analyses suggest that incomplete lineage sorting and/or introgression has further confounded the phylogenetic placements of additional species including C. nebrius, C. vestigium, C. insularis, C. grismeri, and perhaps G. copei. Despite many independent instances of interspecific hybridization among crotaphytid lizards, the species continue to maintain morphological and geographic cohesiveness throughout their ranges.

Morphology, molecules, and the phylogenetics of cetaceans.

Recent phylogenetic analyses of cetacean relationships based on DNA sequence data have challenged the traditional view that baleen whales (Mysticeti) and toothed whales (Odontoceti) are each monophyletic, arguing instead that baleen whales are the sister group of the odontocete family Physeteridae (sperm whales). We reexamined this issue in light of a morphological data set composed of 207 characters and molecular data sets of published 12S, 16S, and cytochrome b mitochondrial DNA sequences. We reach four primary conclusions: (1) Our morphological data set strongly supports the traditional view of odontocete monophyly; (2) the unrooted molecular and morphological trees are very similar, and most of the conflict results from alternative rooting positions; (3) the rooting position of the molecular tree is sensitive to choice of artiodactyls outgroup taxa and the treatment of two small but ambiguously aligned regions of the 12S and 16S sequences, whereas the morphological root is strongly supported; and (4) combined analyses of the morphological and molecular data provide a well-supported phylogenetic estimate consistent with that based on the morphological data alone (and the traditional view of toothed-whale monophyly) but with increased bootstrap support at nearly every node of the tree.

Quantifying ecological, morphological, and genetic variation to delimit species in the coast horned lizard species complex (Phrynosoma)

Lineage separation and divergence form a temporally extended process whereby populations may diverge genetically, morphologically, or ecologically, and these contingent properties of species provide the operational criteria necessary for species delimitation. We inferred the historical process of lineage formation in the coast horned lizard (Phrynosoma coronatum) species complex by evaluating a diversity of operational species criteria, including divergence in mtDNA (98 specimens; 2,781 bp) and nuclear loci (RAG−1, 1,054 bp; BDNF 529 bp), ecological niches (11 bioclimatic variables; 285 unique localities), and cranial horn shapes (493 specimens; 16 landmarks). A phylogenetic analysis of mtDNA recovers 5 phylogeographic groups arranged latitudinally along the Baja California Peninsula and in California. The 2 southern phylogeographic groups exhibit concordance between genetic, morphological, and ecological divergence; however, differentiation is weak or absent at more recent levels defined by phylogeographic breaks in California. Interpreting these operational species criteria together suggests that there are 3 ecologically divergent and morphologically diagnosable species within the P. coronatum complex. Our 3-species taxonomic hypothesis invokes a deep coalescence event when fitting the mtDNA genealogy into the species tree, which is not unexpected for populations that have diverged recently. Although the hypothesis that the 3 phylogeographic groups distributed across California each represent distinctive species is not supported by all of the operational species criteria evaluated in this study, the conservation status of the imperiled populations represented by these genealogical units remains critical.

Molecular Phylogenetics and the Diversification of Hummingbirds

The tempo of species diversification in large clades can reveal fundamental evolutionary mechanisms that operate on large temporal and spatial scales. Hummingbirds have radiated into a diverse assemblage of specialized nectarivores comprising 338 species, but their evolutionary history has not, until now, been comprehensively explored. We studied hummingbird diversification by estimating a time-calibrated phylogeny for 284 hummingbird species, demonstrating that hummingbirds invaded South America by ∼22 million years ago, and subsequently diversified into nine principal clades (see [5-7]). Using ancestral state reconstruction and diversification analyses, we (1) estimate the age of the crown-group hummingbird assemblage, (2) investigate the timing and patterns of lineage accumulation for hummingbirds overall and regionally, and (3) evaluate the role of Andean uplift in hummingbird speciation. Detailed analyses reveal disparate clade-specific processes that allowed for ongoing species diversification. One factor was significant variation among clades in diversification rates. For example, the nine principal clades of hummingbirds exhibit ∼15-fold variation in net diversification rates, with evidence for accelerated speciation of a clade that includes the Bee, Emerald, and Mountain Gem groups of hummingbirds. A second factor was colonization of key geographic regions, which opened up new ecological niches. For example, some clades diversified in the context of the uplift of the Andes Mountains, whereas others were affected by the formation of the Panamanian land bridge. Finally, although species accumulation is slowing in all groups of hummingbirds, several major clades maintain rapid rates of diversification on par with classical examples of rapid adaptive radiation.