William S. Moore

A phylogenomic study of birds reveals their evolutionary history.

Deep avian evolutionary relationships have been difficult to resolve as a result of a putative explosive radiation. Our study examined ∼32 kilobases of aligned nuclear DNA sequences from 19 independent loci for 169 species, representing all major extant groups, and recovered a robust phylogeny from a genome-wide signal supported by multiple analytical methods. We documented well-supported, previously unrecognized interordinal relationships (such as a sister relationship between passerines and parrots) and corroborated previously contentious groupings (such as flamingos and grebes). Our conclusions challenge current classifications and alter our understanding of trait evolution; for example, some diurnal birds evolved from nocturnal ancestors. Our results provide a valuable resource for phylogenetic and comparative studies in birds.

Inferring Phylogenies from mtDNA Variation: Mitochondrial-Gene Trees Versus Nuclear-Gene Trees

An accurately resolved gene tree may not be congruent with the species tree because of lineage sorting of ancestral polymorphisms. DNA sequences from the mitochondrially encoded genes (mtDNA) are attractive sources of characters for estimating the phylogenies of recently evolved taxa because mtDNA evolves rapidly, but its utility is limited because the mitochondrial genes are inherited as a single linkage group (haplotype) and provide only one independent estimate of the species tree. In contrast, a set of nuclear genes can be selected from distinct chromosomes, such that each gene tree provides an independent estimate of the species tree. Another aspect of the gene‐tree versus species‐tree problem, however, favors the use of mtDNA for inferring species trees. For a three‐species segment of a phylogeny, the branching order of a gene tree will correspond to that of the species tree if coalescence of the alleles or haplotypes occurred in the internode between the first and second bifurcation. From neutral theory, it is apparent that the probability of coalescence increases as effective population size decreases. Because the mitochondrial genome is maternally inherited and effectively haploid, its effective population size is one‐fourth that of a nuclear‐autosomal gene. Thus, the mitochondrial‐haplotype tree has a substantially higher probability of accurately tracking a short internode than does a nuclear‐autosomal‐gene tree. When an internode is sufficiently long that the probability that the mitochondrial‐haplotype tree will be congruent with the species tree is 0.95, the probability that a nuclear‐autosomalgene tree will be congruent is only 0.62. If each of k independently sampled nuclear‐gene trees has a probability of congruence with the species tree of 0.62, then a sample of 16 such trees would be required to be as confident of the inference based on the mitochondrial‐haplotype tree. A survey of mtDNA‐haplotype diversity in 34 species of birds indicates that coalescence is generally very recent, which suggests that coalescence times are typically much shorter than internodal branch lengths of the species tree, and that sorting of mtDNA lineages is not likely to confound the species tree. Hybridization resulting in transfer of mtDNA haplotypes among branches could also result in a haplotype tree that is incongruent with the species tree; if undetected, this could confound the species tree. However, hybridization is usually easy to detect and should be incorporated in the historical narrative of the group, because reticulation, as well as cladistic events, contributed to the evolution of the group.

Phylogenomic evidence for multiple losses of flight in ratite birds

Ratites (ostriches, emus, rheas, cassowaries, and kiwis) are large, flightless birds that have long fascinated biologists. Their current distribution on isolated southern land masses is believed to reflect the breakup of the paleocontinent of Gondwana. The prevailing view is that ratites are monophyletic, with the flighted tinamous as their sister group, suggesting a single loss of flight in the common ancestry of ratites. However, phylogenetic analyses of 20 unlinked nuclear genes reveal a genome-wide signal that unequivocally places tinamous within ratites, making ratites polyphyletic and suggesting multiple losses of flight. Phenomena that can mislead phylogenetic analyses, including long branch attraction, base compositional bias, discordance between gene trees and species trees, and sequence alignment errors, have been eliminated as explanations for this result. The most plausible hypothesis requires at least three losses of flight and explains the many morphological and behavioral similarities among ratites by parallel or convergent evolution. Finally, this phylogeny demands fundamental reconsideration of proposals that relate ratite evolution to continental drift.

CHAPTER 4 – The Window of Taxonomic Resolution for Phylogenies Based on Mitochondrial Cytochrome b

The chapter focuses on problems associated with resolving mt-haplotype trees from DNA sequence data. Specifically, it assesses the value of cytochrome b gene (cyt b ) as a source of characters for inferring avian phylogenies, and tries to determine a window in the systematic hierarchy of birds where cyt b sequence should result in the efficient resolution of phylogenetic relationships. The mitochondrially encoded cyt b gene is good for avian systematics, but its utility is greatest in resolving the diversification of birds from the level of species (or subspecies) to subfamilies, and families in some instances. At higher taxonomic levels, cyt b might provide some resolution, but sequencing another gene may be a better investment. In birds, diverging cyt b sequences accrue transition substitutions at a rapid, and more or less constant, rate to the level of distinct genera within tribes, and transversions continue to accrue in a similar manner to the approximate level of superfamilies. These substitutions are primarily synonymous as evidenced by a comparison of the synonymous and nonsynonymous substitution columns. Rather than verifying every nucleotide for a single specimen by sequencing both DNA strands, it is better to sequence one strand for two specimens, thus, keeping the cost the same but greatly reducing the chances of reporting a contaminant sequence.

STABILITY OF THE NORTHERN FLICKER HYBRID ZONE IN HISTORICAL TIMES: IMPLICATIONS FOR ADAPTIVE SPECIATION THEORY

The hybrid zone between the Red‐ and Yellow‐shafted Flickers has been stable on the United States Great Plains in historical times. This conclusion is based on multivariate comparisons of historical and contemporary collections from 18 locales. Adaptive speciation theory predicts that the hybrid zone should either become broader or narrower as a result of introgressive hybridization or reinforcement of premating isolating mechanisms. Neither of these predictions was borne out. Despite 10,000‐13,000 years of hybridization, mating between subspecies remains indiscriminate. The data are also inconsistent with a dynamicequilibrium hypothesis wherein narrow hybrid zones are maintained by hybrid unfitness. According to this hypothesis, the hybrid zone would probably “flow” unless it was trapped by a population density trough. The hybrid zone does not appear to be associated with such a feature.

Coexistence in Unisexual-Bisexual Species Complexes of Poeciliopsis (Pisces: Poeciliidae)

All—female forms of Poeciliopsis rely on males of closely related bisexual species for sperm. The natural habitat of Poeciliopsis in Sonora Mexico, consists of a variety of small ponds connected by intermittent watercourses. Optimal areas, containing mixed female aggregates, are defended by territorial males. Social structure in natural populations very closely resembles that of laboratory experiments, wherein subordinant males show reduced mate discrimination and inseminate unisexuals. An equation relating male density to unisexual inseminations is used in a computer simulation model of a population. A stable equilibrium is inherent in unisexual—bisexual species complexes but the level of equilibrium is affected by the environment. Coexistence does not require niche separation. The simulations predict the percentage of unisexuals pregnant in natural populations and explain their distribution pattern. The strength of the mechanism is demonstrated by a natural population in which the percentage of unisexua...

RANDOM MATING IN THE NORTHERN FLICKER HYBRID ZONE: IMPLICATIONS FOR THE EVOLUTION OF BRIGHT AND CONTRASTING PLUMAGE PATTERNS IN BIRDS

The Red‐shafted and Yellow‐shafted Flickers hybridize in a narrow zone on the western Great Plains of North America. The two subspecies are markedly different in six plumage traits. Plumage phenotypes were scored for the male and female of 125 mated pairs from the hybrid zone.

Evidence for selection against hybrids in the family cyprinidae (Genus Notropis)

Notropis cornutus and N. chrysocephalus are two cyprinid fishes which hybridize extensively in the midwest. In this paper, statistical analysis was used to determine if the deficiency of Notropis cornutus × N. chrysocephalus hybrids can be attributed partly to selection against hybrids. Principal component analysis was used to construct a folded hybrid index (FHI) using morphological and electrophoretic characters which distinguish N. cornutus, N. chrysocephalus, and their hybrids. A Wilcoxon signed‐rank test comparing mean FHI between successive age classes within cohorts and regression analysis of FHI on age supported the conclusion that hybrids are less fit than parentals in nature; however, this analysis did not include a test of selection at zygotic and larval life history stages or partial infertility of hybrids. Selection eliminated hybrids at a rate of 9.2% per year. Considering the intensity of selection and the age of hybridization, it is surprising that premating reproductive isolating mechanisms have not been perfected by selection against gametic wastage as predicted by classical speciation theory. It appears that the reinforcement of premating isolating mechanisms is an extremely slow process, if it occurs at all, despite apparently intense selection against hybrids.

A single locus mass-action model of assortative mating, with comments on the process of speciation

SummaryGenes that cause positive assortative mating have the potential of effecting reproductive isolation and hence speciation. A one-locus-2-allele model of assortative mating is investigated. In this model, when two individuals encounter, they mate with probability 1, α or β depending on whether they share 2, 1 or 0 alleles respectively at the assortative mating locus. The special case where α = 0·5; β = 0 is investigated extensively. Assortative mating eliminates genetic polymorphisms. The only non-trivial equilibrium occurs when each homozygote has a frequency of 0·5 and there are no heterozygotes, but this equilibrium is unstable. Numerical analysis suggests that this is also true when assortment is only partial (β>0). When the alleles are allowed to mutate from one form to the other, a stable non-trivial equilibrium results, but one allele or the other is very rare. When the alleles affect fitness in some additional way, the assortative mating locus will be polymorphic provided there is substantial hybrid superiority; e.g. when the homozygotes are equally fit, the heterozygote must be approximately twice as fit. Similarly, favourable mutants at the assortative mating locus cannot enter a population unless they enhance the fitness of both their genotypes rather substantially. Thus, in the hypothesis of speciation where premating isolating mechanisms are supposed to evolve as a response to selection against hybrids, there is some doubt as to whether genetic variation for assortative mating would exist, and, if it did, whether it would always respond to selection.

Parsimony and Model-Based Analyses of Indels in Avian Nuclear Genes Reveal Congruent and Incongruent Phylogenetic Signals

Insertion/deletion (indel) mutations, which are represented by gaps in multiple sequence alignments, have been used to examine phylogenetic hypotheses for some time. However, most analyses combine gap data with the nucleotide sequences in which they are embedded, probably because most phylogenetic datasets include few gap characters. Here, we report analyses of 12,030 gap characters from an alignment of avian nuclear genes using maximum parsimony (MP) and a simple maximum likelihood (ML) framework. Both trees were similar, and they exhibited almost all of the strongly supported relationships in the nucleotide tree, although neither gap tree supported many relationships that have proven difficult to recover in previous studies. Moreover, independent lines of evidence typically corroborated the nucleotide topology instead of the gap topology when they disagreed, although the number of conflicting nodes with high bootstrap support was limited. Filtering to remove short indels did not substantially reduce homoplasy or reduce conflict. Combined analyses of nucleotides and gaps resulted in the nucleotide topology, but with increased support, suggesting that gap data may prove most useful when analyzed in combination with nucleotide substitutions.