Kevin E. Omland

EXAMINING TWO STANDARD ASSUMPTIONS OF ANCESTRAL RECONSTRUCTIONS: REPEATED LOSS OF DICHROMATISM IN DABBLING DUCKS (ANATINI)

Although phylogenetic reconstruction of ancestral character states is becoming an increasingly common technique for studying evolution, few researchers have assessed the reliability of these reconstructions. Here I test for congruence between a phylogenetic reconstruction and a widely accepted scenario based on independent lines of evidence. I used Livezeys (1991) phylogeny to reconstruct ancestral states of plumage dichromatism in dabbling ducks (Anatini). Character state mapping reconstructs monochromatic ancestors for the genus Anas as well as most of its main clades. This reconstruction differs strongly from the widely accepted scenario of speciation and plumage evolution in the group (e.g., Delacour and Mayr 1945; Sibley 1957). This incongruence may occur because two standard assumptions of character state reconstruction are probably not met in this case. Violating either of these two assumptions would be a source of error sufficient to create misleading reconstructions. The first assumption that probably does not apply to ducks is that terminal taxa, in this case species, are monophyletic. Many of the widespread dichromatic species of ducks may be paraphyletic and ancestral to isolated monochromatic species. Three lines of evidence support this scenario: population‐level phylogenies, biogeography, and vestigial plumage patterns. The second assumption that probably does not apply to duck plumage color is that gains and losses of character states are equally likely. Four lines of evidence suggest that dichromatic plumage might be lost more easily than gained: weak female preferences for bright male plumage, biases toward the loss of sexually dichromatic characters, biases toward the loss of complex characters, and repeated loss of dichromatism in other groups of birds. These seven lines of evidence support the accepted scenario that widespread dichromatic species repeatedly budded off isolated monochromatic species. Drift and genetic biases probably caused the easy loss of dichromatism in ducks and other birds during peripatric speciation. In order to recover the accepted scenario using Livezeys tree, losses of dichromatism must be five times more likely than gains. The results of this study caution against the uncritical use of unordered parsimony as the sole criterion for inferring ancestral states. Detailed population‐level sampling is needed and altered transformation weighting may be warranted in ducks and in many other groups and character types with similar attributes.

NUCLEAR LOCI AND COALESCENT METHODS SUPPORT ANCIENT HYBRIDIZATION AS CAUSE OF MITOCHONDRIAL PARAPHYLY BETWEEN GADWALL AND FALCATED DUCK (ANAS SPP.)

Abstract Many species have mitochondrial DNA lineages that are phylogenetically intermixed with other species, but studies have rarely tested the cause of such paraphyly. In this study, we tested two hypotheses that could explain mitochondrial paraphyly of Holarctic gadwalls (Anas strepera) with respect to Asian falcated ducks (A. falcata). First, hybridization could have resulted in falcated duck mitochondrial DNA (mtDNA) introgressing into the gadwall gene pool. Second, gadwalls and falcated ducks could have diverged so recently that mtDNA lineages have not sorted to reciprocal monophyly. We used coalescent analyses of three independent loci to distinguish between these two hypotheses. Two lines of evidence support introgression. First, analyses of the three loci combined show that some introgression is necessary to explain current genetic diversity in gadwalls. Second, we generated alternative predictions regarding time since divergence estimated from mtDNA: falcated ducks and gadwalls would have diverged between 65,000 and 700,000 years before present (ybp) under the introgression hypothesis and between 11,000 and 76,000 ybp under the incomplete lineage sorting hypothesis. The two independent nuclear introns indicated that these species diverged between 210,000 and 5,200,000 ybp, which did not overlap the predicted time for incomplete lineage sorting. These analyses also suggested that ancient introgression (∼14,000 ybp) has resulted in the widespread distribution and high frequency of falcated-like mtDNA (5.5% of haplotypes) in North America. This is the first study to use a rigorous quantitative framework to reject incomplete lineage sorting as the cause of mitochondrial paraphyly.

CORRELATED RATES OF MOLECULAR AND MORPHOLOGICAL EVOLUTION

Since Zuckerkandl and Pauling (1962, 1965) proposed the molecular clock, many studies seem to have supported their prediction that rates of molecular and morphological evolution generally will be decoupled. Most of these studies were aimed at taxa in which rates of morphological evolution were thought to vary greatly a priori. For the current survey eight diverse taxa were systematically chosen from published studies without regard to prior expectations about rates. Two approaches showed that rates of molecular and morphological evolution may usually be coupled. First, correlations in the total number of changes accumulated in terminal taxa suggest that some mechanism alters the rates of both morphological and molecular evolution in concert. Second, node‐density effects were removed statistically, and average corrected base‐to‐tip totals were compared among sister clades. Across all taxa 50 of 72 of these corrected contrasts support the hypothesis that rates of molecular and morphological evolution are correlated; this finding is highly significant by a binomial test. Furthermore, there were positive correlations between inferred molecular and morphological branch lengths in seven of eight cases, which is also significant. These branch length correlations are consistent with the rate correlations, and suggest that amounts of molecular and morphological evolution often are correlated also. This study supports the assumptions of several phylogenetic methods, and highlights a need for new inquiries into many aspects of both molecular and morphological evolution.

Female song is widespread and ancestral in songbirds

Bird song has historically been considered an almost exclusively male trait, an observation fundamental to the formulation of Darwins theory of sexual selection. Like other male ornaments, song is used by male songbirds to attract females and compete with rivals. Thus, bird song has become a textbook example of the power of sexual selection to lead to extreme neurological and behavioural sex differences. Here we present an extensive survey and ancestral state reconstruction of female song across songbirds showing that female song is present in 71% of surveyed species including 32 families, and that females sang in the common ancestor of modern songbirds. Our results reverse classical assumptions about the evolution of song and sex differences in birds. The challenge now is to identify whether sexual selection alone or broader processes, such as social or natural selection, best explain the evolution of elaborate traits in both sexes.

Genetic signatures of intermediate divergence: population history of Old and New World Holarctic ravens ( Corvus corax )

Many studies of phylogeography, speciation, and species limits restrict their focus to a narrow issue: gene tree monophyly. However, reciprocal monophyly does not provide an ideal touchstone criterion of any aspect of evolutionary divergence. There is a continuum of divergence stages as isolated populations go from initial allele frequency differences to well‐differentiated species. Studying intermediate stages of divergence will increase our understanding of geographical speciation, species limits, and conservation priorities. We develop a conceptual framework and terminology for thinking about the stages of ‘intermediate polyphyly’. The Holarctic clade of common ravens (Corvus corax), found throughout much of Eurasia and North America, provides a case study of these stages of intermediate divergence. We used coalescent, phylogenetic, and population genetic methods to investigate the history and current status of this Old World–New World distribution using 107 mitochondrial control region sequences. Phylogenetically, New World and Old World samples are intermixed. However, most samples are grouped into small subclades that are restricted to either the New World or the Old World, and only one haplotype is shared between the hemispheres. Analysis of moleculalr variance (amova) results reflect this low haplotype sharing between hemispheres (ΦST = 0.13, P < 0.01). Isolation with Migration (im) coalescent results suggest a sustained period of divergence between the hemispheres and low levels of maternal gene flow. Although there has not been sufficient time to evolve reciprocal monophyly and some gene flow may occur, New World and Old World ravens are genetically quite distinct. We use this example to demonstrate these early stages of divergence as populations go from sharing only internal haplotypes, to sharing no haplotypes, to having population specific subclades. Studies of phylogeography, speciation and systematics will benefit from increased attention to these stages of intermediate polyphyly.

NOVEL INTRON PHYLOGENY SUPPORTS PLUMAGE CONVERGENCE IN ORIOLES (ICTERUS)

Abstract A recent study of New World orioles (Icterus spp.), which traced a large number of plumage characters onto a mitochondrial DNA phylogeny, reported high frequencies of evolutionary convergence and reversal of plumage characters (Omland and Lanyon 2000). Although those results are consistent with other smaller scale studies that have documented plumage homoplasy, the mitochondrial genome is inherited as a single linkage group, so mitochondrial data represent only one gene tree. The mitochondrial (mt) DNA tree may not reflect the true evolutionary history of a lineage; therefore, it remains possible that the plumage characters could reflect the true species phylogeny. Other rapidly evolving regions of DNA can provide independent phylogenetic hypotheses useful for evaluating mitochondrial gene trees. A novel phylogenetic marker, a region of the nuclear gene ornithine decarboxylase (ODC) spanning from exon 6 to exon 8, was sequenced in 10 oriole species. The resultant nuclear gene tree reconstructs the same three major oriole clades as the mtDNA tree (Omland et al. 1999), supporting the conclusion that plumage evolution in the New World orioles has been highly homoplastic. Although most phylogenetic studies that have employed introns report greatest resolution at the genus or family level, ODC appears to offer some degree of phylogenetic resolution for infrageneric analyses. However, that intron has clearly not sorted to monophyly within or between closely related species.

Phylogeography: its development and impact in Australo-Papuan ornithology with special reference to paraphyly in Australian birds

Abstract With examples from Australo-Papuan ornithology, we examine the technical and theoretical roots of molecular phylogeography and review its development. We describe the progression from ad hoc interpretation of gene trees in single species phylogeographic studies through to comparative phylogeography and currently advocated model-testing approaches. Mitochondrial DNA (mtDNA) sequences have provided most advances to date, although we demonstrate and advocate the future use of multilocus datasets analysed with coalescent methods. We examine interrelationships among speciation research, historical biogeography, phylogeography and landscape genetics. Mitochondrial paraphyly, in which individuals of one species or population have mtDNA that is more closely related to that of another than to their own, emerges in 44% of Australian studies to date as a common, important result in Australian avian phylogeography. Accordingly, we explore at length its most common causes and its impact on case studies in Australo-Papuan avian phylogeography. The impact of so much paraphyly on avian phylogeography and taxonomy is a major theme of the review. We suggest a full research agenda for avian phylogeography in the Australo-Papuan region that spans diverse topics: the need for more studies of pelagic birds, spatio-temporal links between New Guinea and Australia, island populations, testing of long-established biogeographical hypotheses, and integration of molecular and non-molecular datasets into integrated evolutionary understanding of species and populations. Studying the full continuum of divergences from landscape genetics, to phylogeography, to recently diverged species with evidence of paraphyly, to highly divergent species with many fixed differences will lead to a more complete understanding of the processes and patterns of avian evolution.

Losses of female song with changes from tropical to temperate breeding in the New World blackbirds

Birds in which both sexes produce complex songs are thought to be more common in the tropics than in temperate areas, where typically only males sing. Yet the role of phylogeny in this apparent relationship between female song and latitude has never been examined. Here, we reconstruct evolutionary changes in female song and breeding latitude in the New World blackbirds (Icteridae), a family with both temperate and tropical representatives. We provide strong evidence that members of this group have moved repeatedly from tropical to temperate breeding ranges and, furthermore, that these range shifts were associated with losses of female song more often than expected by chance. This historical perspective suggests that male-biased song production in many temperate species is the result not of sexual selection for complex song in males but of selection against such songs in females. Our results provide new insights into the differences we see today between tropical and temperate songbirds, and suggest that the role of sexual selection in the evolution of bird song might not be as simple as we think.

Late Pleistocene divergence between eastern and western populations of wood ducks ( Aix sponsa ) inferred by the 'isolation with migration' coalescent method

During the Late Pleistocene, glaciers sundered many species into multiple glacial refugia where populations diverged in allopatry. Although deeply divergent mitochondrial DNA (mtDNA) lineages often reflect the number of refugia occupied, it is unlikely that populations that split during the recent Wisconsin glaciations will have reached reciprocal monophyly. We examined mtDNA control region sequences from eastern and western populations of wood ducks (Aix sponsa) to determine whether their current, disjunct distribution is consistent with the occupancy of two glacial refugia. We used the ‘isolation with migration’ coalescent method (im) to simultaneously estimate effective population sizes, maternal gene flow, and time since divergence. We found 24 unique haplotypes, none of which were shared between the eastern and western populations, but we did not find diagnostic monophyletic lineages suggestive of long‐term isolation in multiple glacial refugia. However, a high ΦST (0.31) indicates that eastern and western populations are well differentiated in mtDNA, and results from im suggest that these populations have been diverging, without extensive gene flow, for 10 000 to 124 000 years. Results from im further suggest that these populations most likely split about 34 000 years ago, and this time of divergence is consistent with the occupancy of multiple glacial refugia during the Late Wisconsin glaciation. Eastern wood ducks are characterized by high genetic diversity, a large effective population size, and a recent population expansion, while western wood ducks have much less genetic diversity, a smaller population size, and have not undergone a recent population expansion.

Random interbreeding between cryptic lineages of the Common Raven: evidence for speciation in reverse

DNA sequence studies frequently reveal evidence of cryptic lineages in morphologically uniform species, many of which turn out to be evolutionarily distinct species. The Common Raven (Corvus corax) includes two deeply divergent mtDNA lineages: one lineage seems restricted to western North America and the other is Holarctic in distribution. These deep clades hint of the possibility of cryptic species in the western United States. We tested this hypothesis in a population consisting of an equal proportion of both mtDNA clades, by quantifying mating patterns and associated fitness consequences with respect to mtDNA. We also tested for morphological, behavioural and ecological correlates of sex and mtDNA clade membership. Mate pairings were random with respect to mtDNA clades, and there were no differences in reproductive success between assortatively and nonassortatively mated pairs. We found no differences in survival or resource use between clades. There were no differences in morphological or behavioural characters between mtDNA clades, except one clade trended towards greater mobility. These results suggest there are no barriers to gene flow between mtDNA clades and argue that the mtDNA clades have remerged in this population, likely due to a lack of ecological or signal differentiation between individuals in each lineage. Hence, in Common Ravens, phylogeographic structure in mtDNA is a reflection of likely past isolation rather than currently differentiated species.