Considering the use of the terms strain and adaptation in prion research

Evolutionary biologists and disease biologists use the terms strain and adaptation in Chronic Wasting Disease (CWD) research in different ways. In evolutionary biology, a strain is a nascent genetic lineage that can be described by a genealogy, and a phylogenetic nomenclature constructed to reflect that genealogy. Prion strains are described as showing distinct host range, clinical presentation, disease progression, and neuropathological and PrP biochemical profiles, and lack information that would permit phylogenetic reconstruction of their history. Prion strains are alternative protein conformations, sometimes derived from the same genotype. I suggest referring to prion strains as ecotypes, because the variant phenotypic conformations (“strains”) are a function of the interaction between PRNP amino acid genotype and the host environment. In the case of CWD, a prion ecotype in white-tailed deer would be described by its genotype and the host in which it occurs, such as the H95 þ ecotype. However, an evolutionary nomenclature is difficult because not all individuals with the same PRNP genotype show signs of CWD, therefore creating a nomenclature reflecting and one-to-one relationship between PRNP genealogy and CWD presence is difficult. Furthermore, very little information exists on the phylogenetic distribution of CWD ecotypes in wild deer populations. Adaptation has a clear meaning in evolutionary biology, the differential survival and reproduction of individual genotypes. If a new prion ecotype arises in a particular host and kills more hosts or kills at an earlier age, it is the antithesis of the evolutionary definition of adaptation. However, prion strains might be transmitted across generations epigenetically, but whether this represents adaptation depends on the fitness consequences of the strain. Protein phenotypes of PRNP that cause transmissible spongiform encephalopathies (TSEs), and CWD, are maladaptive and would not be propagated genetically or epigenetically via a process consistent with an evolutionary view of adaptation. I suggest terming the process of prion strain origination “phenotypic transformation”, and only adaptation if evidence shows they are not maladaptive and persist over evolutionary time periods (e.g., thousands of generations) and across distinct species boundaries (via inheritance). Thus, prion biologists use strain and adaptation, historically evolutionary terms, in quite different ways

Phylogenetic Tests of Models of Viral Transmission

The hunt for the immediate non-human host of SARS-CoV-2 has centered on bats of the genus Rhinolophus. We explored the phylogenetic predictions of two models of viral transmission, the SpilloverModel and the CirculationModel and suggest that the Spillover Model can be eliminated. The Circulation Model suggests that viral transmission occurs among susceptible hosts irrespective of their phylogenetic relationships. Susceptibility could be mediated by the ACE2 gene (important for viral docking) and we constructed a phylogeny of this gene for 159 mammal species, finding a phylogenetic pattern consistent with established mammalian relationships. The tree indicates that viral transfer occurs over large evolutionary distances. Although lacking consensus, some studies identify a virus from a particular R. affinis individual (RaTG13) as being most closely related phylogenetically to human SARS-CoV-2. However, other R. affinis harbor viruses that are relatively unrelated to human viruses, and viruses found in this species exhibit sequence differences of up to 20%, suggesting multiple transfers over time. There is little correspondence between viral and host (bat) species limits or phylogenetic relationships. An ACE2 phylogeny for Rhinolophus followed species limits, unlike the pattern in the viral phylogeny indicating that phylogenetic similarity of ACE2 is not a predictor of viral transmission at the bat species level. The Circulation Model could be modified to apply to any individual of any species of Rhinolophus; more individuals and species must be examined

Geographic variation, null hypotheses, and subspecies limits in the California Gnatcatcher: A response to McCormack and Maley

We interpreted the results of nuclear DNA sequencing to be inconsistent with the recognition of California Gnatcatcher (Polioptila californica) subspecies. McCormack and Maley (2015) suggested that our data did support 2 taxa, one of which was P. c. californica, listed as Threatened under the Endangered Species Act (ESA). We summarize here how 2 sets of researchers with access to the same data reached different conclusions by including different analyses. We included the southern subspecies’ boundary from the taxonomy of Atwood (1991), the taxonomic basis for the ESA listing, which resulted in an Analysis of Molecular Variance that provided no support for subspecies. In contrast, using a novel taxonomic hypothesis without precedent in the literature, McCormack and Maley (2015) found statistically significant FST values for 2 loci, which they suggested supports P. c. californica. We propose that our mitochondrial and nuclear data had sufficient power to capture geographical structure at either the phylogenetic (monophyly) or traditional ‘‘75% rule’’ level. McCormack and Maley (2015) suggested that finding an absence of population structure was a ‘‘negative result,’’ whereas we consider it to be the null hypothesis for a species with gene flow and no geographical barriers. We interpret the unstructured mtDNA and nuclear DNA trees, the STRUCTURE analysis supporting one group, the identification of just 26% (and not 75%) of individuals of P. c. californica with the most diagnostic nuclear locus, the overall GST that suggests that over 98% of the variation is explained by nontaxonomic sources, and the lack of evidence of ecological differentiation to indicate that P. c. californica is not a valid subspecies. McCormack and Maley (2015) suggest that statistically significant differences at 2 loci that explained ,6% of the genetic variation, and previous morphological data, support recognition of P. c. californica. If ornithology continues to recognize subspecies, these different standards should be reconciled

PHYLOGEOGRAPHY OF THE CALIFORNIA GNATCATCHER (POLIOPTILA CALIFORNICA) USING MULTILOCUS DNA SEQUENCES AND ECOLOGICAL NICHE MODELING: IMPLICATIONS FOR CONSERVATION

An important step in conservation is to identify whether threatened populations are evolutionarily discrete and significant to the species. A prior mitochondrial DNA (mtDNA) phylogeographic study of the California Gnatcatcher (Polioptila californica) revealed no geographic structure and, thus, did not support the subspecies validity of the threatened coastal California Gnatcatcher (P. c. californica). The U.S. Fish and Wildlife Service concluded that mtDNA data alone were insufficient to test subspecies taxonomy. We sequenced eight nuclear loci to search for historically discrete groupings that might have been missed by the mtDNA study (which we confirmed with new ND2 sequences). Phylogenetic analyses of the nuclear loci revealed no historically significant groupings and a low level of divergence (GST = 0.013). Sequence data suggested an older population increase in southern populations, consistent with niche modeling that suggested a northward range expansion following the Last Glacial Maximum (LGM). The signal of population increase was most evident in the mtDNA data, revealing the importance of including loci with short coalescence times. The threatened subspecies inhabits the distinctive Coastal Sage Scrub ecosystem, which might indicate ecological differentiation, but a test of niche divergence was insignificant. The best available genetic, morphological, and ecological data indicate a southward population displacement during the LGM followed by northward range expansion, without the occurrence of significant isolating barriers having led to the existence of evolutionarily discrete subspecies or distinct population segments that would qualify as listable units under the Endangered Species Act

Niche modeling reveals life history shifts in birds at La Brea over the last twenty millennia

A species presence at a particular site can change over time, resulting in temporally dynamic species pools. Ecological niche models provide estimates of species presence at different time intervals. The avifauna of La Brea includes approximately 120 species dating to approximately 15,000 years ago. Niche models predicted presence at the Last Glacial Maximum for over 90% of 89 landbird species. This confirms that niche modeling produces sensible range estimates at the Last Glacial Maximum. For 97 currently local species that are as yet undocumented at La Brea over 90% were predicted to occur; absence is due to insufficient study, lack of the ecological niche, transient occurrence or a behavioral ability to avoid entrapment. Our 366 niche models provide a prospective checklist of the landbird fauna of La Brea. The models indicate fluidity in life history strategies and a higher proportion of resident birds at the LGM (88% to 60%). We evaluated a subset of 103 species in breeding and winter periods using two climate models (MIROC−ESM, CCSM4) with a variety of differing parameters, finding differences in 5% of the niche models. Niche breadths in bark-foraging birds changed little between the present and LGM, suggesting that greater species diversity at the LGM was due to greater niche availability rather than contractions of niche breadths (i.e., niche partitioning)

A Cytochrome-b Perspective on Passerina Bunting Relationships

We sequenced the complete mitochondrial cytochrome-b gene (1,143 nucleotides) for representatives of each species in the cardinalid genera Passerina (6 species), Guiraca (1 species), and Cyanocompsa (3 species), and used a variety of phylogenetic methods to address relationships within and among genera. We determined that Passerina, as presently recognized, is paraphyletic. Lazuli Bunting (P. amoena) is sister to the much larger Blue Grosbeak (Guiraca caerulea). Indigo Bunting (P. cyanea) and Lazuli Bunting are not sister taxa as generally thought. In all weighted parsimony trees and for the gamma-corrected HKY tree, Indigo Bunting is the sister of two sister groups, a “blue” (Lazuli Bunting and Blue Grosbeak) and a “painted” (Rosita\u27s Bunting [P. rositae], Orange-breasted Bunting [P. leclancherii], Varied Bunting [P. versicolor], and Painted Bunting [P. ciris]) clade. The latter two species form a highly supported sister pair of relatively more recent origin. Uncorrected (p) distances for ingroup (Passerina and Guiraca) taxa range from 3.0% (P. versicolor–P. ciris) to 7.6% (P. cyanea–P. leclancherii) and average 6.5% overall. Assuming a molecular clock, a bunting “radiation” between 4.1 and 7.3 Mya yielded four lineages. This timing is consistent with fossil evidence and coincides with a late-Miocene cooling during which a variety of western grassland habitats evolved. A reduction in size at that time may have allowed buntings to exploit that new food resource (grass seeds). We speculate that the Blue Grosbeak subsequently gained large size and widespread distribution as a result of ecological character displacement

Nanostructure and mechanics of mummified type I collagen from the 5300-year-old Tyrolean Iceman

Skin protects the body from pathogens and degradation. Mummified skin in particular is extremely resistant to decomposition. External influences or the action of micro-organisms, however, can degrade the connective tissue and lay the subjacent tissue open. To determine the degree of tissue preservation in mummified human skin and, in particular, the reason for its durability, we investigated the structural integrity of its main protein, type I collagen. We extracted samples from the Neolithic glacier mummy known as ‘the Iceman’. Atomic force microscopy (AFM) revealed collagen fibrils that had characteristic banding patterns of 69 ± 5 nm periodicity. Both the microstructure and the ultrastructure of dermal collagen bundles and fibrils were largely unaltered and extremely well preserved by the natural conservation process. Raman spectra of the ancient collagen indicated that there were no significant modifications in the molecular structure. However, AFM nanoindentation measurements showed slight changes in the mechanical behaviour of the fibrils. Young's modulus of single mummified fibrils was 4.1 ± 1.1 GPa, whereas the elasticity of recent collagen averages 3.2 ± 1.0 GPa. The excellent preservation of the collagen indicates that dehydration owing to freeze-drying of the collagen is the main process in mummification and that the influence of the degradation processes can be addressed, even after 5300 years

Evolutionary patterns of morphometrics, allozymes and mitochondrial DNA in thrashers (Genus Toxostoma)

We examined patterns of variation in skeletal morphometrics (29 characters), allozymes (34 loci), mitochondrial DNA (mtDNA) restriction sites (n = 74) and fragments (n = 395), and mtDNA sequences (1,739 bp from cytochrome b, ND2, ND6, and the control region) among all species of Toxostoma. The phenetic pattern of variation in skeletal morphometrics generally matched traditional taxonomic groupings (based on plumage patterns) with the exceptions of T. redivivum, which because of its large size clusters outside of its proper evolutionary group (lecontei), and T. occelatum, which did not cluster with T. curvirostre. Skull characters contributed highly to species discrimination, suggesting that unique feeding adaptations arose in different species groups. Although genetic variation was detected at isozyme loci (average heterozygosity = 3.6%), these data yielded little phylogenetic resolution. Similarly, mtDNA restriction sites were relatively uninformative; hence, phylogenetic conclusions were based on sequence data. Phylogenetic analyses confirmed the monophyly of these traditionally recognized assemblages: rufum group (T. rufum, T. longirostre, and T. guttatum), lecontei group (T. lecontei, T. crissale, and T. redivivum), and cinereum group (T. bendirei and T. cinereum). The cinereum and lecontei groups appear to be sister lineages. Monophyly of the curvirostre group (which also includes T. occelatum) was not confirmed. Sequence data suggest that T. occelatum and T. curvirostre, which differ by 7.7% sequence divergence, are probably most closely related to the rufum group. Toxostoma rufum and T. longirostre have similar external appearances and differ by 5.0%. Toxostoma guttatum is restricted to Cozumel Island and often is considered a subspecies of T. longirostre; it differs by more than 5% from the other two members of the rufum group and is a distinct species constituting the basal member of this group. The phenotypically distinctive T. bendirei and T. cinereum differ in sequence divergence by only 1.6%. Overall, mtDNA distances computed from coding genes (mean 8.5%) exceeded distances computed from the control region (mean 7.6%), contrary to expectation. Because neither allozymes nor mtDNA could unambiguously resolve the placement of T. occelatum and T. curvirostre, a scenario involving contemporaneous speciation is suggested. Application of a molecular clock suggested that most speciation occurred in the late Pliocene or early Pleistocene

Evidence supporting the recent origin and species status of the Timberline Sparrow

The Timberline Sparrow (Spizella taverneri), although originally described as a species, is currently classified as a subspecies of the more widespread Brewer\u27s Sparrow (S. breweri). We investigated the taxonomic status and recent evolutionary history of these species by comparison of both morphological and molecular characters. Morphometric comparisons using 6 external and 18 skeletal measurements show that S. taverneri specimens from two widely separated populations (Yukon and southwestern Alberta, Canada) are indistinguishable with respect to size yet are significantly larger (by 3%) than representatives of several breweri populations. Analysis of 1,413 base pairs of mitochondrial DNA (mtDNA) for 10 breweri and 5 taverneri samples representing widely scattered breeding populations revealed a maximum divergence among any breweri-taverneri pair of 0.21% and an overall average of 0.13%. In contrast, the average (± SE) pairwise distance among the other Spizella species is 5.7 ± 0.5%. We discovered that breweri and taverneri could be distinguished on the basis of a single, fixed nucleotide difference. Of an additional 11 taverneri and 8 breweri surveyed for this diagnostic site, a single bird (morphologically a taverneri) from northwest British Columbia did not sort to type. Overall, 18 of 18 breweri and 15 of 16 taverneri were diagnosable. We interpret these results to suggest that gene flow does not currently occur between these two forms and that each is on an independent, albeit recently derived, evolutionary course. The molecular data are consistent with theoretical expectations of a Late Pleistocene speciation event. We believe that for passerine birds, this is the first empirical validation of this widely accepted evolutionary model. The data presented corroborate plumage, vocal, and ecological evidence suggesting that these taxa are distinct. As such, we suggest that Spizella taverneri be recognized as a species

The taxonomic rank of Spizella taverneri: A response to Mayr and Johnson

Mayr and Johnson suggest that Spizella taverneri should be a subspecies of the biological species S. breweri, because it is possibly not reproductively isolated. We originally concluded that evidence from mitochondrial DNA sequences, habitat preferences, timing of breeding, vocalizations, and morphology supported the recognition of S. taverneri as a phylogenetic and biological species. Nothing in the commentary by Mayr and Johnson causes us to change that conclusion. We believe that it is probable that these two allopatric taxa are isolated. Contrary to Mayr and Johnson, we believe that more information is given by ranking S. taverneri as a species, because it reveals the fact that they are independently evolving taxa. The classification of Spizella should convey the sister-species status of S. taverneri and S. breweri, without regard for balancing the degree of sequence divergence among species, as suggested by Mayr and Johnson