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5 March 2014 Species taxonomy of birds: Which null hypothesis?
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The polytypic species concept unites populations that theoretically could and would interbreed were the opportunity to arise. This concept places the burden of proof of reproductive incapability and species status on those claiming species or higher rank. Advances in our understanding of the nature of reproductive isolation, the genetics of speciation, the limited role of gene flow, the power of directional selection, and the dynamics of hybridization support a different null hypothesis for taxonomic decisions, one that places the burden of proof on ‘lumping' rather than on ‘splitting' taxa at the species level. Switching the burden of proof provides an improved conceptual basis for the recognition of many allopatric island taxa and subspecies groups that merit species status. Taxonomic revisions based on these advances predictably confirm that distinct sister populations once lumped as polytypic species are independent evolutionary lineages that exhibit essential reproductive isolation. Release from the concerns about hybridization also positions proposed species for timely taxonomic decisions. The stage is set to proactively redefine polytypic species to separate component species for the 21st century. The improved species classification will better reflect phylogeny and evolutionary status, characterize biodiversity more accurately, guide improved sampling patterns of bird populations for systematic studies, and enable informed conservation decisions.

Seventy years ago, Ernst Mayr (1942, 1954, 1963) steered the species taxonomy of the world's birds onto a new course with a brilliant integration of classical Drosophila genetics, population genetics, and landmark studies of the systematics of island birds based on museum specimens (Futuyma 1994, Gill 1994, Bock and Lein 2005). Together, he and other leaders of the time launched the “Modern Synthesis” with a vision of polytypic species based on population biology and genetics rather than on typology (O'Hara 1997, Birkhead et al. 2014). Mayr championed the Biological Species Concept (BSC), which portrays species as arrays of local populations that are linked reproductively through exchange of individuals and/or their gametes and progeny (Hastings and Harrison 1994, De Queiroz 2005). Under the BSC, biological species are broad and dynamic entities, or metapopulations, united cohesively by gene flow in geographical space and in evolutionary time and isolated from other such evolutionary lineages. Thus, “biological species are genetically cohesive groups of populations that are reproductively isolated from other such groups” (AOU 1998:xiv).

In practice, species are split by inferences of reproductive isolation or lumped based on evidence of hybridization, phenotypic similarity, or imagined reproductive compatibility. Evolution of reproductive isolation during periods of reduced gene flow has been the foundation of geographical speciation theory. The criterion of reproductive isolation for species status, however, has broadened in recent years to include populations that exhibit “essential reproductive isolation” (AOU 1998:xiv, Johnson et al. 1999), or “substantial but not necessarily complete reproductive isolation” (Coyne and Orr 2004:30). Hybridizing sister taxa exhibit “essential reproductive isolation” when assortative mating, hybrid inferiority, or other departures from free interbreeding restrict gene flow between them. Departures from free interbreeding prove to be more prevalent and more subtle than our predecessors realized, as I review below. Taxonomic practice, therefore, must continue to accommodate advances in understanding “how properties of genomes, organisms and environments lead to restrictions in gene flow” (Harrison 2012:4).

The Biological Species Concept has long guided taxonomic practice in ornithology, despite decades of discomfort and of proposed alternatives (Cracraft 1989, Gill 1995, Johnson et al. 1999, Coyne and Orr 2004, Remsen 2005, Peterson and Navarro-Sigüenza 2006, Zink 2006). In contrast to revisions of higher-level taxonomy, the contests among taxonomic camps seem to have constrained major revisions of species limits of birds. Ornithologists, however, are not as polarized in the actual practice of taxonomy as one might think. The concept of species as independent evolutionary lineages unifies all species concepts at a primary level, even though operational criteria for delimiting lineages may differ (De Queiroz 2007). Applications of lineage concepts usually include diagnostic characters of morphology and vocalizations that contribute to essential reproductive isolation. Considerations of multiple criteria, such as diagnosability, lineage monophyly, and species recognition blend strict applications of different species concepts into an integrated practice (Payne and Sorenson 2007, Irestedt et al. 2013). Publications in avian taxonomy increasingly accommodate alternative species concepts in the same paragraph and treat different criteria as complementary rather than competitive (Tobias et al. 2010, Sangster 2009, 2013). Features of diagnosability (emphasized under the Phylogenetic Species Concept) actually prevail over assessments of reproductive isolation and the degree of difference as criteria for deciding taxonomic rank for subspecies and species (Sangster 2013). Applications of the Biological Species Concept increasingly incorporate empirical delimitations of lineage independence, the hallmark of the Evolutionary Species Concept. Together, these factors predictably reveal that populations of birds once lumped within polytypic species are independent evolutionary lineages that qualify as species under all three concepts.

Allopatric populations, including those on separate mountains and other disjunct habitats as well as those on oceanic islands, have challenged Biological Species Concept taxonomy since its initial formulation because, among other issues, one cannot assess reproductive isolation between them (Mayr 1940, Zink and McKitrick 1995, Helbig et al. 2002, Remsen 2010, Tobias et al. 2010, Winker 2010). Whether they be Island Thrushes (Turdus poliocephalus) of the western Pacific or montane populations of Common Bush Tanagers (Chlorospingus flavopectus) of the Neotropics, differentiated “island” populations aggregate into bloated polytypic species that comprise diagnosable, independent, evolutionary lineages (Peterson 2006, Andersen 2013a). These lineages often qualify for (biological) species status, even though we can only guess whether they are reproductively isolated. The realities of reduced gene flow between “island” taxa favor an assumption of essential reproductive isolation as the default condition. In practice, the delimitation of Evolutionary Species Concept lineages converges with applications of the Biological Species Concept for these avifaunas (Andersen et al. 2013b). As a general rule, therefore, many distinct island taxa merit recognition as valid evolutionary species and biological species until new and compelling evidence is presented to the contrary (Pratt 2010; cf. Remsen 2005, 2010).

Null Hypotheses

Explicit null hypotheses add rigor and clarity to the scientific process (Popper 2002, Prum 2010). With respect to species classifications in ornithology based on the Biological Species Concept, the prevailing, usually implicit, null hypothesis is:

  • H01: Distinct and reciprocally monophyletic sister populations of birds do not exhibit essential reproductive isolation and would interbreed freely if they were to occur in sympatry.

Documentation of essential reproductive isolation, such as assortative mating or hybrid inferiority, provides a basis for the rejection of H01 and, in turn, the assignment of species status to divergent populations. Conversely, clinal intergradation and uncompromised introgressive hybridization support H01 and deny separate species status for sister populations. Distinct allopatric populations are lumped by default to await critical study and rejection of H01 through peer-reviewed publication and debate by committees of experts. Proposals for splitting 1 species into 2 or more bear the burden of proof for rejecting H01, regardless of how obviously those taxa may merit species status (Remsen 2005).


An alternative null hypothesis would be:

  • H02: Distinct and reciprocally monophyletic sister populations of birds exhibit essential reproductive isolation and would not interbreed freely if they were to occur in sympatry.

Documentation of free interbreeding is required to reject H02 and to treat divergent sister populations as conspecifics, whereas predictable features of lineage independence and essential reproductive isolation would support acceptance of species status. Divergent allotaxa would be treated as species by default. Proposals to retain the status of two or more distinct sister taxa as a single species bear the burden of proof for rejecting H02, regardless of how subjectively those taxa may have been lumped in the past.

These two null hypotheses are mutually exclusive mirror images of each other. Rejection of H01 is tantamount to acceptance of H02, and vice versa. Choosing one default polarity over the other for operational purposes may seem inconsequential, but there are good reasons to do so. Specifically, advances in knowledge of bird populations and their evolution soundly reject H01 and strongly favor H02 as the appropriate default null hypothesis for future testing and rejection.


Taxonomic decisions are hypotheses about evolutionary relationships and reproductive compatibility of taxa (Zink 2006, Patten 2010). The species taxonomy of birds has benefited from advances in both theory and empirical research (Helbig et al. 2002, Remsen 2010, Yang and Rannala 2010, Reid and Carstens 2012, Sangster 2013). Present understanding of the major features of speciation in birds differs from that used as a basis for formulation of the Biological Species Concept (Table 1). In 1942, little was known about the history and genetic consequences of range expansions, the roles of phylogeny and lineage sorting, the dynamics and power of social selection (including sexual selection), the nature of reproductive isolation in birds, the architecture of avian hybrid zones, or the ecology and genomics of speciation (Edwards et al. 2005, Price 2008, Ellegren 2013, Nosil and Feder 2013). Projections of monophyly, historical dynamics, lineage independence, and profiles of genetic divergence now supplement the classical character sets used in taxonomic studies. Low levels of gene flow between nonsister taxa are relatively common and are therefore a poor indicator of whether two populations should be considered conspecific. Hybridization between distinct biological species is also a widespread and prevalent phenomenon that does not threaten species status (Grant and Grant 1992, Mallet 2007, Harrison 2012).

Mayr (1942, 1963) viewed species as dynamic populations of individuals stabilized by shared coadaptive gene complexes. Special events were thought to overcome the intrinsic forces of cohesion. Advances in the empirical genetics of bird populations, however, reject the three pillars of Mayr's model of speciation genetics—genetic revolutions, founder effects, and genetic drift. These factors are not driving features of avian speciation (Coyne and Orr 2004, Edwards et al. 2005). Genetic revolutions do not overcome the assumed inertia of coadapted gene complexes and epistasis (Lande 1980). Instead, essential reproductive isolation evolves through simple, additive effects of new genes. Furthermore, founder effects and genetic drift during colonization do not drive genetic diversity or divergence of bird populations, at least to the extent that was once assumed (Barton and Mallet 1996, Clegg et al. 2002a, Walsh et al. 2005, Price 2008, Balakrishnan and Edwards 2009). Modern theory itself imposes stringent conditions on the potential roles of founder effects and drift in adaptive innovation and radiation (Templeton 2008), but empirical support is predictably scarce (Clegg et al. 2002a, 2002b, Grant 2002, Clegg and Phillimore 2010). Models based on divergence with gene flow are replacing the geographical speciation models in general and the long-accepted allopatric speciation model in particular (Fitzpatrick et al. 2008, Harrison 2012, Winker et al. 2013). Coalescence models allow inference regarding recent histories of divergence with variable levels of gene flow (Wakeley 2008, 2010, Hey 2010) and thus deeper insight into the speciation process than was possible with classical constructs based simply on spatial distribution (Harrison 2012).

Our understanding of reproductive isolation in birds also has advanced well beyond the ingredients of the Modern Synthesis, which emphasized postzygotic isolation. Neither genetic divergence as espoused by Mayr nor the intrinsic postzygotic barriers championed by Dobzhansky (1951) prevail as key features of the speciation process in birds. Unlike mammals and fruit flies, birds typically retain genomic compatibility, hybrid viability, and fertility for millions of years (Prager and Wilson 1975, Edwards et al. 2005, Price 2008, González et al. 2009). Complete loss of F1 hybrid fertility in birds takes millions of years; hybrid inviability takes longer to manifest by an order of magnitude. Even nonsister species and those in different genera of ducks, fowl, hummingbirds, buntings, and others hybridize successfully. Consequently, the propensity of birds to evolve intrinsic reproductive isolation does not predict the rate at which they form new species over geological timescales (Rabosky and Matute 2013). Instead, birds speciate before they achieve hybrid sterility or hybrid inviability (Price and Bouvier 2002, Lijtmaer et al. 2003, Edwards et al. 2005).

Prezygotic incompatibilities, including those in social signals and ecology, are the primary ingredients of essential reproductive isolation in birds (Edwards et al. 2005, Price 2008). Postzygotic reduction of hybrid fitness—including disparities in courtship behavior, migration patterns, habitats, and ecological physiology, or genetic incompatibilities in backcross generations—supports the evolution of prezygotic isolating mechanisms. Sexual selection and social selection lead the speciation process in birds, mediated by cultural processes such as imprinting and song learning (Zink 1996, Paterson 1985, Carling and Brumfield 2008, Price 2008). Advances in genomics focus on the roles of sex-linked genes, including Haldane's Rule, and speciation genes that control traits such as plumage and vocalizations (Edwards et al. 2005, Wolf et al. 2010, Nosil and Schluter 2011). Mutations of regulatory and “switch” genes bypass the hypothesized barriers of epistasis to effect significant changes in prezygotic compatibility. Local adaptive shifts to new climates, habitats, temporal cycles, and assemblages of species also may promote reproductive isolation (Funk et al. 2006, Price 2008, Schluter 2009, Nosil 2012).

Hybridization and Essential Reproductive Isolation

Regarding the interpretation of hybridization, we emphasize that a significant number of undisputed biological species of birds long retain the capacity for at least limited interbreeding with other species, even non-sister taxa (Prager and Wilson 1975, Grant and Grant 1992). Therefore, the occasional occurrence of hybridization, even between taxa that the Committee has long recognized as species, by no means diminishes the biological reality of their essential reproductive isolation. In practice, interbreeding has not been the ironclad determinate of conspecificity that some would believe. Thus, essential (lack of free interbreeding) rather than complete reproductive isolation has been and continues to be the fundamental operating criterion for species status by workers adhering to the BSC. (AOU 1998:xiv)

Advances in understanding of the speciation process, including the prevalence and consequences of interspecific hybridization among birds, reaffirm the (American Ornithologists' Union's [AOU's]) policy of dismissing narrow hybrid zones as evidence of conspecificity. More broadly, the extent and consequences of hybridization are not easily assessed. They add little value to species threshold decisions, even beyond the Phylogenetic Species Concept view that hybridization is a shared, ancestral feature (see Remsen 2005, Zink 2006 for points/counterpoints). {Note: I confine the term ‘hybridization' to interbreeding between distinct taxa that actually or potentially qualify for species rank (McCarthy 2006), as opposed to broad (clinal) intergradation among populations traditionally treated as subspecies.}

First, hybridization by undisputed bird species is widespread (Grant and Grant 1992). Well-documented cases of it rarely invalidate species status in ornithology, with few exceptions. In one case, the Blue Goose (Anser caerulescens) and Snow Goose (Anser [Chen] hyperborea) were essentially allopatric in distribution until ∼70 years ago, when their populations expanded. Now they are sympatric and behave as a single species, with extensive gene flow causing the color types to vary in frequency across much of the species' range (Mowbray et al. 2000). Ornithologists retain many separate species that hybridize with extensive introgression. Widespread, interspecific hybridization by waterfowl (Anseriformes), usually incidental but sometimes extensive, does not threaten status as a species (Tubaro and Lijtmaer 2002, McCarthy 2006, Winker et al. 2013). Unambiguous species, such as the (introduced) Mallard (Anas platyrhynchos) and Pacific Black (Gray) Duck (A. superciliosa) in New Zealand, hybridize extensively with extensive bilateral introgression (Rhymer et al. 1994, Williams and Basse 2006), to the extent that Pacific Black Ducks are in danger of extinction in New Zealand due to genetic assimilation and ecological replacement by Mallards. No authorities consider them to be conspecific. Similar cases abound on the most authoritative regional and world bird lists.

Second, modern studies of the genetic architecture of avian hybrid zones typically reveal a lack of free interbreeding by some combination of assortative mating, subtle selection against hybrids, ecological displacement, or gene-dependent introgression (Harrison 1993). Essential reproductive isolation is the expected and default condition in hybrid zones; few sister taxa of birds interbreed freely or fuse via zones of secondary contact. Instead, hybrid zones serve as population sinks or tension zones that reflect ecological and other fitness differences among parental genotypes and their hybrid offspring (Moore and Price 1993, Wiebe 2000). Rarely also does interspecific hybridization lead to hybrid speciation, as in the Audubon's Warbler (Setophaga [coronata] auduboni; Brelsford et al. 2011) and Italian Sparrow (Passer italiae; Elgvin et al. 2011, Hermansen et al. 2011), although admittedly this phenomenon may be underestimated because of the difficulties of demonstrating it (Harrison 2012). More often, one expanding taxon eliminates the other following transient or wave front hybridization accompanied, or not, by assimilation or incorporation of some genes of the replaced taxon (Rhymer and Simberlof 1996, Rohwer et al. 2001, Gill 2004).

Third, introgression due to interspecific hybridization contributes advantageously and more extensively to speciation than was previously recognized (Dowling and Secor 1997, Rheindt and Edwards 2011). The “semipermeable” genetic architecture of hybrid zones allows free exchange of some genes and genomes, but not others that are subject to negative selection (Harrison 2012). Neutral (nuclear) genes, for example, are more likely to be introgressive than mtDNA genes due to Haldane's Rule or selection against sex-linked genes in the heterogametic sex (e.g., Carling and Brumfield 2008). Alternatively, advantageous mtDNA of one species may sweep through and replace that of the other species as a positive source of climatic adaptation (Zink and Barrowclough 2008, McKay and Zink 2010, Rheindt and Edwards 2011). Even low or episodic pulses of hybridization between divergent sister species can provide beneficial gene exchange without fusion (Weckstein et al. 2001, Peters et al. 2013, Toews et al. 2013).

Essential reproductive isolation is the well-established prognosis for candidate species even when hybridization is reported, yet debates about species status still defer to concerns about hybridization in contact zones. For example, consider the fate of the model AOU's proposal (NACC 2009-A-2) to split the Woodhouse's Jay (Aphelocoma [californica] woodhousei) from the Western Scrub-Jay (Aphelocoma californica). It failed to achieve the two-thirds majority of votes by committee members that is required for approval. The defining question was: How much hybridization takes place between Woodhouse's Jays and California Jays in a small, but unstudied, contact zone in the Pine Nut Mountains of extreme western Nevada? The prevailing (5/12) ‘No' votes focused on possible hybridization because, to paraphrase committee comments posted on the AOU's website (, ‘what occurs in that narrow zone of contact is a critical and underdeveloped aspect of an otherwise strong case for species status.' Recent studies of the jays in the contact zone support the majority prediction of restricted introgression and species status (Gowen et al. 2012). A backlog of such cases of undecided species status awaits attention (AOU 1998, Hockey et al. 2006, Christidis and Boles 2008, Remsen 2013).

The advances in the documentation of hybridization and its consequences in birds negate its value as a primary criterion for conspecificity. The burden of proof should fall instead on the explicit definition and documentation of free interbreeding. Given today's standards, historical samples of hybrid specimens from localities of presumed secondary contact are not sufficient to judge whether two taxa interbreed freely. Required instead are field studies that fully take into account (1) subtle forms of selection against hybrids (Brelsford and Irwin 2009), (2) variable dynamics of introgression of nuclear DNA and mtDNA genes, including selection against some but not others, (3) paternity issues that cloud assessments of levels of hybridization and assortative mating based on field observations of socially paired birds (Gill 2004, Vallender et al. 2007), (4) geographical mosaics in the amount of essential isolation, (5) time lines of transient hybridization, and (6) the positive consequences of interspecific introgression between taxa that continue to be recognized as biological species.

Gene Flow and Selection

Ornithologists loosely invoke gene flow as a criterion for conspecificity. Although sometimes significant (Kisel and Barraclough 2010), gene flow generally does not explain phenotypic uniformity at large scales, nor does it unite allopatric bird populations as cohesively as was hypothesized in the Modern Synthesis. However, rigorous metrics are still needed for defining how much actual gene flow is, or is not, allowed between recognized species. Stringent theoretical conditions underpin the hypothesis that gene flow is a powerful force of cohesion; these conditions are not often manifest in natural populations (Miles and Allendorf 2002). Inadequate time to complete lineage sorting and to diverge by natural selection is responsible for many patterns of genetic uniformity that previously were attributed to cohesive gene flow or panmixia (Rheindt and Edwards 2011). Instead, speciation histories are revealed by partitioning ancestral retention of genes from estimates of current gene flow (Hung et al. 2012). Historically recent range expansions or replacements of locally extinct (sink) populations are responsible for the lack of genetic population structure of many widespread, seemingly highly mobile species (Diamond 1980, Mayr and Diamond 2001, Clegg and Phillimore 2010). Thus, populations of temperate zone species that have expanded their ranges since the last glaciations tend to be unstructured or to carry signatures of their historical refugia (Gill et al. 1993, Zink 1997, Perktas et al. 2011). Conversely, historically (more) stable, tropical bird species tend to exhibit deeper population structures than their temperate counterparts (Tobias et al. 2008). As a result, phylogeographic population structures may contradict the boundaries of classical subspecies taxonomy (Seutin et al. 1993, Avise 2000).

Many variables reduce the effective exchange of individuals among conspecific populations (potential gene flow) and consequent, or realized, gene flow, i.e. the actual incorporation of immigrant alleles into the gene pool of the recipient population (Futuyma 2009, Harrison 2012). Defined as “reduced survival of immigrants upon reaching foreign habitats that are ecologically divergent from their native habitat” (Nosil et al. 2005:705), immigrant inviability reduces realized gene flow and increases essential reproductive isolation (Grant 2002, Price 2008, Harrison 2012). Immigrants may also be disadvantaged by the physiological costs of dispersal (Harrison 2012). Among the costs, new island colonists are compromised as agents of gene flow from the source population due to reduced prospects for social integration and survival as well as for breeding with established individuals (Clegg 2009). Conversely, established predecessors have an advantage due to prior social selection and adaptations to local diseases, parasites, predators, and other “enemies” (Ricklefs 2005). Pleiotropic effects of the genes involved in ecological adaptations contribute to reduced gene flow and to essential reproductive isolation (Schluter 2009, Nosil 2012). Alternatively, mtDNA genes that directly control physiological adaptations may sweep through founding populations and be closed to future gene flow from source populations by Haldane's Rule (Rheindt and Edwards 2011, Ribeiro et al. 2011).

Finally, gene flow may actually advance the speciation process by increasing genetic variation in recipient populations (Irwin et al. 2001, 2005, Church and Taylor 2002, Gavrilets and Gibson 2002, Toews et al. 2013). In their studies of the potentially opposing trends of “fission” versus “fusion” in Darwin's finches (Geospiza spp.), Grant and Grant (2008a, 2008b, 2010) concluded that gene flow among finch populations does not constrain phenotypic divergence. Conversely, gene flow augments genetic variation and facilitates local evolutionary divergence due to natural selection. The adaptive radiation of Darwin's finches has occurred either despite or, perhaps, thanks to ongoing low levels of gene flow.

It follows that divergence due to natural selection and sexual selection typically trumps uniformity due to cohesive gene flow or divergence due to genetic drift (Barton and Mallet 1996, Coyne and Orr 2004, Phillimore et al. 2008, Clegg and Phillimore 2010, Seddon et al. 2013, Uy et al. 2013). Even modest directional selection for heritable traits overrides gene flow at surprisingly local geographical scales and climatic gradients (Gill 1973, Postma and Noordwijk 2005, Clegg and Phillimore 2010, Milá et al. 2010, Sly et al. 2011, Myers et al. 2012, VanderWerf 2012). New colonists of island environments are generally promptly subject to directional selection both for generic traits of island songbirds, including shorter wings and longer bills, and for new social and ecological relationships (Wright and Steadman 2012).

Episodes of directional selection affect the evolution of bird populations more dramatically than was envisioned in the early days of the Modern Synthesis. In their classic studies of Darwin's finches in the Galápagos Islands, Grant and Grant (2008a) documented the pulses of intense natural selection on the local populations. El Niño–Southern Oscillation (ENSO) cycles of drought and rainfall cause dramatic changes in seed sizes and availabilities that favor individuals of different bill sizes, which in turn affects individual vocalizations and mate choice. Like the Galápagos finches, the population of Silver-eyes (Zosterops lateralis) on Heron Island off northeastern Australia experiences major pulses of selection due to tropical cyclones and ENSO climate cycles (Clegg et al. 2008). In this case, pioneering Silver-eyes and their descendants responded initially to directional selection with a shift to a new optimum phenotype, followed by stabilization under generally weak directional selection.

In summary, the role of gene flow as a dominant source of cohesion in bird populations has been overestimated. Empirical data on the genetic structure of bird populations highlight the roles of historical range expansions and directional selection in defining patterns and pace of geographic variation and the potential for speciation. Bird populations respond to directional selection at greater intensities and at more local geographical scales than was fully appreciated in the formulation of the Modern Synthesis.

The Polytypic Species Concept Revisited

Many mergers in the early days of the biological species concept were not based on strong biological evidence. We have retained the merged species because in most instances strong evidence for re-division has not been presented. (AOU 1998:xii)

The number of extant bird species recognized currently ranges from 9,721 (Dickinson 2003) to 10,507 (Gill and Donsker 2013). Dozens of species are added each year with discoveries of new cryptic species and as we chip away at the backlog of polytypic species. However, the stage is set to boldly revisit polytypic species worldwide with the goal of partitioning avian diversity consistently and comprehensively into species units that correspond more closely to their evolutionary history, current geography, and ecology. The backlog of polytypic species awaiting attention due to historical inertia is large, and the pace of taxonomic decisions—some straightforward, some difficult—is painfully slow (Navarro-Sigüenza and Peterson 2004). Proposals to separate polytypic species into component and valid species are handicapped by an inadequate workforce, insufficient modern specimen resources, stringent documentation of hallowed species status, and adherence to an obsolete null hypothesis. Can we instead move forward predictively based on the body of case studies of speciation in birds, and especially the advances of the past 30 years? Can we compile an improved working baseline of distinct bird taxa that meets approved criteria for species status based on a default prediction of essential reproductive isolation? Bird taxonomy, of course, is not the only discipline being challenged; so too is the taxonomy of other classes of vertebrates. For example, Rana pipiens is now 28 species (Moore 1944, Pace 1974, Hillis 1988, Newman et al. 2012) and Plethodon glutinosus is now at least 16 contiguous species (Highton et al. 1989).

Our “modern” classification of bird species remains rooted in morphological descriptions of new taxa that accumulated throughout the 19th century to a zenith of 18,937 (Sharpe 1909, Allen 1910). Aggregation of conspecific age and sex classes, seasonal plumages, and geographical subspecies followed the growth of museum collections and maturing of scientific ornithology from 1900 to 1940, including Robert Ridgway's (and Herbert Friedmann's) insightful work, The Birds of North and Middle America (1901–1950). But then the eager application of a broad polytypic species concept caused wholesale lumping of similar allopatric taxa. The world list of birds shrank to a nadir of 8,616 (Mayr 1946, Mayr and Amadon 1951). In particular, Peters' Checklist of Birds of the World—the cornerstone of 20th century ornithology—left a legacy of polytypic species that regrettably distorts estimates of biodiversity, speciation, and conservation status (Pratt 2010, Tobias et al. 2010).

Maintaining what we know to be wrong in the name of conservative stability is not an appropriate option. Fortunately, a new era of analysis of polytypic taxa is under way. Fully empowered studies predictably reveal distinct species that have long been buried as subspecies. Details of genetic divergence, biogeography, plumage patterns, and vocalizations provide improved criteria for species diagnosis. Recent examples include Philippine owls (Miranda et al. 2011, Rasmussen et al. 2012), Thrush-like Schiffornis (Schiffornis spp.) of Latin America (Nyári 2007, Remsen 2013), Scytalopus tapaculos of the Andes (Krabbe and Cadena 2010, Hosner et al. 2013b), and many others. Phylogenetic analyses unravel colonization histories, independent lineages, and patterns of speciation (Reddy 2008, Rheindt and Eaton 2009, Perktas et al. 2011, Sánchez-González and Moyle 2011, Andersen et al. 2013a, 2013b, Hosner et al. 2013a, Irestedt et al. 2013). Rigorous sets of evolutionary lineages replace the original projections of reproductive isolation and evolutionary independence. Differences between sympatric, congeneric species in morphology and vocalizations, supplemented by DNA divergences, help us to calibrate new thresholds of species status (Isler et al. 1998, Helbig et al. 2002, Tobias et al. 2010, Amei and Smith 2013). The revised classifications, which in the New World will resurrect the insights of Robert Ridgway and other giants on whose shoulders we stand, better reflect phylogeny and evolutionary status, more accurately define biodiversity, guide improved DNA sampling patterns of bird populations, and enable informed conservation management (Peterson 2006, De Queiroz 2007).

Maintaining the criteria and publication process for managing descriptions of newly discovered cryptic species of antpittas and tapaculos, among others, is an ongoing and vital process that continues strong traditions. At the other end of the spectrum, however, are famously bloated polytypic species such as the Horned Lark (Eremophila alpestris; 42 subspecies) and Island Thrush (Turdus poliocephalus; 51 subspecies). In 1 such case, the 15 allopatric subspecies of the Variable Dwarf Kingfisher (Ceyx lepidus) of western Pacific islands are morphologically distinct and genetically more differentiated (2.6–6.8% based on ND2 sequences) than 2 closely related sister species. All are eligible for species rank (Andersen et al. 2013b). Similarly, the island populations of the Red-bellied Pitta (Erythropitta erythrogaster) may comprise 17 or more species (Irestedt et al. 2013). Regionally, the avifauna of the Philippine islands is rich in classical polytypic species that arguably are among the most overlumped in the world (Peterson 2006, Collar 2011, Brown et al. 2013). The region's bird list grew slowly at first from 450 species (Delacour and Mayr 1946) to 572 (Kennedy et al. 2000), but renewed fieldwork supplemented by DNA analyses of speciation and historical biogeography is fragmenting species complexes into their components. Both recent discoveries of new species and revisions of polytypic species have added dozens of species to this avifauna in the last 10 years, with many more to come (Sánchez-González and Moyle 2011, Rasmussen et al. 2012, Andersen et al. 2013a, 2013b, Hosner et al. 2013a, 2013b).

How then can we proceed boldly as a discipline of taxonomic progress, not taxonomic inflation (Sangster 2009)? Improved standardization and transparency of species taxonomy, informed by current research, is essential (Helbig et al. 2002, Remsen 2005). Advances in our knowledge of birds, however, favors acceptance of essential reproductive isolation and lineage independence as default expectations in the practice of species taxonomy. Acceptance of this strongly supported proposition would move aside the anchors of hybridization analysis and classical deference to possible gene flow. Most importantly, we would be able to take command of the legacy of polytypic species that distorts the taxonomy of birds. Yes, defaulting to H02 will occasionally produce splits that will be reversed upon further study, but occasional, correctible oversplitting is preferable to continuing the inertia and inappropriate lumping of valid bird species.

Adoption of this working proposition will accelerate the inventory of species to a needed new baseline founded on consistent application of consensus-based metrics of species taxonomy within an improved framework of a unified species concept and an informed null hypothesis. Taxonomic decisions must be independent of their applications in research and conservation. Accordingly, species recognized via the proposed default hypothesis will be more useful on average for current research than are today's recognized species, which tend to obscure variations that evolutionary biologists, ecologists, behaviorists, and conservation biologists find interesting and important. From a purely practical standpoint, changing the null hypothesis will shift priorities to studies of the genetic architecture of speciation instead of continuing to confirm predictions of essential reproductive isolation. Finally, and best of all, conservation priorities will be based on an improved foundation of avian diversity, genetics, and evolution (Rojas-Soto et al. 2010). The birds themselves will benefit from one small paradigm shift that embraces the advances in ornithology that Ernst Mayr himself spearheaded 70+ years ago. The remaining birds of the world deserve no less.


Many thanks to the following colleagues who greatly improved this manuscript: David Donsker, Douglas Futuyma, Douglas Gill, Peter Grant, Richard Klim, Scott Lanyon, Town Peterson, Douglas Pratt, Pamela Rasmussen, Robert Zink, and two anonymous reviewers. Mistakes of understanding or attribution remain my own, with apologies.


  1. J. A Allen (1910). Sharpe's hand-list of birds. The Auk 27:93–95. Google Scholar
  2. A Ameiand B. T Smith (2013). Robust estimates of divergence times and selection with a Poisson random field model: A case study of comparative phylogeographic data. Genetics: Early Online. doi: 10.1534/genetics.113.157776 Google Scholar
  3. M. J Andersen A Nyári I Mason L Joseph J. P Dumbacher C. E Filardiand R. G Moyle (2013a). Molecular systematics of the world's most polytypic bird: The Pachycephala pectoralis/melanura (Aves: Pachycephalidae) species complex. Zoological Journal of the Linnean Society 169. doi: 10.1111/zoj.12088 Google Scholar
  4. M. J Andersen C. H Oliveros C. E Filardiand R. G Moyle (2013b). Phylogeography of the Variable Dwarf Kingfisher Ceyx lepidus (Aves: Alcedinidae) inferred from mitochondrial and nuclear DNA sequences. The Auk 130:118–131. Google Scholar
  5. AOU (1998). Check-list of North American Birds. 7th edition. American Ornithologists' Union, Washington D.C., USA. Google Scholar
  6. J. C Avise (2000). Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, MA, USA. Google Scholar
  7. C. N Balakrishnanand S. V Edwards (2009). Nucleotide variation, linkage disequilibrium and founder-facilitated speciation in wild populations of the Zebra Finch (Taeniopygia guttata). Genetics 181:645–660. Google Scholar
  8. N. H Bartonand J Mallet (1996). Natural selection and random genetic drift as causes of evolution on islands. Philosophical Transactions of the Royal Society B 351:785–795. Google Scholar
  9. T Birkhead J Wimpennyand B Montgomerie (2014). Ten Thousand Birds: Ornithology since Darwin. Princeton University Press, Princeton, NJ, USA. Google Scholar
  10. W Bockand R Lein (2005). Ernst Mayr at 100: Ornithologist and Naturalist. Ornithological Monographs 58. Google Scholar
  11. A Brelsfordand D. E Irwin (2009). Incipient speciation despite little assortative mating: The Yellow-rumped Warbler hybrid zone. Evolution 63:3050–3060. Google Scholar
  12. A Brelsford B Miláand D. E Irwin (2011). Hybrid origin of Audubon's Warbler. Molecular Ecology 20:2380–2389. Google Scholar
  13. R. M Brown C. D Siler C. H Oliveros J. A Esselstyn A. C Diesmos P. A Hosner C. W Linkem A. J Barley J. R Oaks M. B Sanguila L. J Welton D. C Blackburn et al . (2013). Evolutionary processes of diversification in a model island archipelago. Annual Review of Ecology, Evolution, and Systematics 44:411–435. Google Scholar
  14. M. D Carlingand R. T Brumfield (2008). Haldane's Rule in an avian system: Using cline theory and divergence population genetics to test for differential introgression of mitochondrial, autosomal, and sex-linked loci across the Passerina bunting hybrid zone. Evolution 62:2600–2615. Google Scholar
  15. L Christidisand W. E Boles (2008). Systematics and taxonomy of Australian birds. CSIRO Publishing, Collingwood, Australia. Google Scholar
  16. S. A Churchand D. R Taylor (2002). The evolution of reproductive isolation in spatially structured populations. Evolution 56:1859–1862. Google Scholar
  17. S. M Clegg (2009). Empirical Insights into the Roles of Microevolutionary Processes. In The Theory of Island Biogeography Revisited ( J. B Lososand R. E Ricklefs Editors). Princeton University Press, Princeton, NJ, USA. pp. 293–325. Google Scholar
  18. S. M Cleggand A. B Phillimore (2010). The influence of gene flow and drift on genetic and phenotypic divergence in two species of Zosterops in Vanuatu. Philosophical Transactions of the Royal Society B 365:1077–1092. Google Scholar
  19. S. M Clegg S. M Degnan J Kikkawa C Moritz A Estoupand I. P. F Owens (2002a). Genetic consequences of sequential founder events by an island-colonizing bird. Proceedings of the National Academy of Sciences USA 99:8127–8132. Google Scholar
  20. S. M Clegg S. M Degnan C Moritz J Kikkawa A Estoupand I. P. F Owens (2002b). Microevolution in island forms: The roles of drift and directional selection in morphological divergence of a passerine bird. Evolution 56:2090–2099. Google Scholar
  21. S. M Clegg D. F Frentiu J Kikkawa G Tavecchiaand I. P. F Owens (2008). 4000 years of phenotypic change in an island bird: Heterogeneity of selection over three microevolutionary timescales. Evolution 62:2393–2410. Google Scholar
  22. N. J Collar (2011). Species limits in some Philippine birds including the Greater Flameback Chrysocolaptes lucidus. Forktail 27:29–38. Google Scholar
  23. J. A Coyneand H. A Orr (2004). Speciation. Sinauer Associates, Sunderland, MA, USA. Google Scholar
  24. J Cracraft (1989). Speciation and its ontology: The empirical consequences of alternative species concepts for understanding patterns and processes of differentiation. In Speciation and Its Consequences ( D Otteand J Endler Editors). Sinauer Associates, Sunderland, MA, USA. pp. 28–59. Google Scholar
  25. J Delacourand E Mayr (1946). Birds of the Philippines. Macmillan, New York, NY, USA. Google Scholar
  26. K De Queiroz (2005). Ernst Mayr and the modern concept of species. Proceedings of the National Academy of Sciences USA 102:6600–6607. Google Scholar
  27. K De Queiroz (2007). Species concepts and species delimitation. Systematic Biology 56:879–886. Google Scholar
  28. J Diamond (1980). Species turnover in island bird communities. In Acta XVII Congressus Internationalis Ornithologica ( R Nöhring Editor). Verlag der Deutschen Ornithologen-Gesellschaft, Berlin, Germany. pp. 777–782. Google Scholar
  29. E. C Dickinson (Editor) (2003). The Howard and Moore Complete Checklist of the Birds of the World. 3rd Edition. Princeton University Press, Princeton, NJ, USA. Google Scholar
  30. T Dobzhansky (1951). Genetics and the Origin of Species. 3rd Edition. Columbia University Press, New York, NY, USA. Google Scholar
  31. T. E Dowlingand C. L Secor (1997). The role of hybridization and introgression in the diversification of animals. Annual Review of Ecology and Systematics 28:593–619. Google Scholar
  32. S. V Edwards S. B Kingan J. D Calkins C. N Balakrishnan W. B Jennings W. J Swansonand M. D Sorenson (2005). Speciation in birds: Genes, geography, and sexual selection. Proceedings of the National Academy of Sciences USA 102(Supplement 1):6550–6557. Google Scholar
  33. T. O Elgvin J. S Hermansen A Fijarczyk T Bonnet T Borge S. A Sæther K. L Vojeand G.-P Sætre (2011). Hybrid speciation in sparrows II: A role for sex chromosomes? Molecular Ecology 20:3823–3837. Google Scholar
  34. H Ellegren (2013). The evolutionary genomics of birds. Annual Review of Ecology, Evolution, and Systematics 44:239–259. Google Scholar
  35. B. M Fitzpatrick J. H. A Fordyceand S Gavrilets (2008). What, if anything, is sympatric speciation? Journal of Evolutionary Biology 21:1452–1459. Google Scholar
  36. D. J Funk P Nosiland W. J Etges (2006). Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proceedings of the National Academy of Sciences USA 103:3209–3213. Google Scholar
  37. D. J Futuyma (1994). Ernst Mayr and evolutionary biology. Evolution 48:36–43. Google Scholar
  38. D. J Futuyma (2009). Evolution. 2nd Edition. Sinauer Associates, Sunderland, MA, USA. Google Scholar
  39. S Gavriletsand N Gibson (2002). Fixation probabilities in a spatially heterogeneous environment. Population Ecology 44:51–58. Google Scholar
  40. F. B Gill (1973). Intra-island variation in the Mascarene White-eye Zosterops borbonica. Ornithological Monographs 12. Google Scholar
  41. F. B Gill (1994). Ernst Mayr, the ornithologist. Evolution 48:12–18. Google Scholar
  42. F. B Gill (1995). Ornithology. 3rd Edition. W. H. Freeman, New York, NY, USA. Google Scholar
  43. F. B Gill (2004). Blue-winged Warblers (Vermivora pinus) vs. Golden-winged Warblers (V. chrysoptera). The Auk 121:1014–1018. Google Scholar
  44. F. B Gilland D Donsker (Editors) (2013). IOC World Bird List (version 3.5). doi: 10.14344/IOC.ML.3.5. Google Scholar
  45. F. B Gill A Mostromand A. L Mack (1993). Speciation in North American chickadees: I. Patterns of mtDNA genetic divergence. Evolution 47:195–212. Google Scholar
  46. J. H González H Düttmannand M Wink (2009). Phylogenetic relationships based on two mitochondrial genes and hybridization patterns in Anatidae. Journal of Zoology 279:310–318. Google Scholar
  47. F Gowen C Cicero A. T Petersonand J McCormack (2012). A genetic portrait of divergence and gene flow between two lineages of Western Scrub-Jay (Aphelocoma californica) based on mitochondrial and nuclear markers. North American Ornithological Congress V:PS1.107. Google Scholar
  48. B. R Grantand P. R Grant (2008a). Fission and fusion of Darwin's finches populations. Philosophical Transactions of the Royal Society B 363:2821–2829. Google Scholar
  49. P. R Grant (2002). Founder effects and Silvereyes. Proceedings of the National Academy of Sciences USA 99:7818–7820. Google Scholar
  50. P. R Grantand B. R Grant (1992). Hybridization of bird species. Science 256:193–197. Google Scholar
  51. P. R Grantand B. R Grant (2008b). How and Why Species Multiply: The Radiation of Darwin's Finches. Princeton University Press, Princeton, NJ, USA. Google Scholar
  52. P. R Grantand B. R Grant (2010). Conspecific versus heterospecific gene exchange between populations of Darwin's finches. Philosophical Transactions of the Royal Society B 365:1065–1076. Google Scholar
  53. R. G Harrison (1993). Hybrid Zones and the Evolutionary Process. Oxford University Press, New York, NY, USA. Google Scholar
  54. R. G Harrison (2012). The language of speciation. Evolution 66:3643–3657. Google Scholar
  55. A Hastingsand S Harrison (1994). Metapopulation dynamics and genetics. Annual Review of Ecology and Systematics 25:167–188. Google Scholar
  56. A. J Helbig A. G Knox D. T Parkin G Sangsterand M Collinson (2002). Guidelines for assigning species rank. Ibis 144:518–525. Google Scholar
  57. J. S Hermansen S. A Saether T. O Elgvin T Borge E Huelleand G.-P Sætre (2011). Hybrid speciation in sparrows I: Phenotypic intermediacy, genetic admixture and barriers to gene flow. Molecular Ecology 20:3812–3822. Google Scholar
  58. J Hey (2010). Isolation with migration models for more than two populations. Molecular Biology and Evolution 27:905–920. Google Scholar
  59. R Highton G. C Mahaand L. R Maxson (1989). Biochemical evolution of the slimy salamander of the Plethodon glutinosus complex in the eastern United States. Illinois Biological Monographs 57. University of Illinois Press, Urbana, IL, USA. Google Scholar
  60. D. M Hillis (1988). Systematics of the Rana pipiens complex: Puzzle and paradigm. Annual Review of Systematics and Ecology 19:39–63. Google Scholar
  61. P. A. R Hockey W. R. J Deanand P. G Ryan (2006). Roberts Birds of Southern Africa. 7th Edition. Trustees of the John Voelcker Bird Book Fund, Cape Town, South Africa. Google Scholar
  62. P. A Hosner A. S Nyáriand R. G Moyle (2013a). Water barriers and intra-island isolation contribute to diversification in the insular Aethopyga sunbirds (Aves: Nectariniidae). Journal of Biogeography 40:1094–1106. Google Scholar
  63. P. A Hosner M. B Robbins T Valquiand A. T Peterson (2013b). A new species of Scytalopus tapaculo (Aves: Passeriformes: Rhinocryptidae) from the Andes of central Peru. Wilson Journal of Ornithology 125:233–242. Google Scholar
  64. C.-M Hung S. V Drovetskiand R. M Zink (2012). Multilocus coalescence analyses support a mtDNA-based phylogeographic history for a widespread Palearctic passerine bird, Sitta europaea. Evolution 66:2850–2864. Google Scholar
  65. M Irestedt P.-H Fabre H Batalha-Filho K. A Jønsson C. S Roselaar G Sangsterand P. G. P Ericson (2013). The spatiotemporal colonization and diversification across the Indo-Pacific by a ‘great speciator' (Aves, Erythropitta erythrogaster). Proceedings of the Royal Society B 280:20130309.  10.1098/rspb.2013.0309 Google Scholar
  66. D. E Irwin S Bensch J. H Irwinand T. D Price (2005). Speciation by distance in a ring species. Science 307:414–415. Google Scholar
  67. D. E Irwin S Benschand T. D Price (2001). Speciation in a ring. Nature 409:333–337. Google Scholar
  68. M. L Isler P. R Islerand B. M Whitney (1998). Use of vocalizations to establish species limits in antbirds (Passeriformes: Thamnophilidae). The Auk 115:577–590. Google Scholar
  69. N. K Johnson J. V Remsen Jrand C Cicero (1999). Resolution of the debate over species concepts in ornithology: A new comprehensive biologic species concept. In Acta XII Congressus Internationalis Ornithologici ( N. J Adamsand R. H Slotow Editors). Birdlife South Africa, Johannesburg, South Africa. pp. 1470–1482. Google Scholar
  70. R. S Kennedy P. C Gonzales E Dickinson H Mirandaand T Fisher (2000). A Guide to the Birds of the Philippines. Oxford University Press, Oxford, UK. Google Scholar
  71. Y Kiseland T. G Barraclough (2010). Speciation has a spatial scale that depends on levels of gene flow. American Naturalist 175:316–334. Google Scholar
  72. N Krabbeand C. D Cadena (2010). A taxonomic revision of the Paramo Tapaculo Scytalopus canus Chapman (Aves: Rhinocryptidae), with a description of a new subspecies from Ecuador and Peru. Zootaxa 2354:56–66. Google Scholar
  73. R Lande (1980). Genetic variation and phenotypic evolution during allopatric speciation. American Naturalist 116:463–479. Google Scholar
  74. D. A Lijtmaer B Mahlerand L Tubaro (2003). Hybridization and postzygotic isolation patterns in pigeons and doves. Evolution 57:1411–1418. Google Scholar
  75. J Mallet (2007). Hybrid speciation. Nature 446:279–283. Google Scholar
  76. E Mayr (1940). Speciation phenomena in birds. American Naturalist 74:249–278. Google Scholar
  77. E Mayr (1942). Systematics and the Origin of Species. Columbia University Press, New York, NY, USA. Google Scholar
  78. E Mayr (1946). The number of species of birds. The Auk 63:64–69. Google Scholar
  79. E Mayr (1954). Change of genetic environment and evolution. In Evolution as a Process ( J Huxley A. J Hardyand E. B Ford Editors). Allen and Unwin, London, UK. pp. 157–180. Google Scholar
  80. E Mayr (1963). Animal Species and Evolution. Belknap Press of Harvard University Press, Cambridge, MA, USA. Google Scholar
  81. E Mayrand D Amadon (1951). A Classification of Recent Birds. American Museum Novitates 1496. American Museum of Natural History, New York, NY, USA. Google Scholar
  82. E Mayrand J Diamond (2001). The Birds of Northern Melanesia: Speciation, Ecology, and Biogeography. Oxford University Press, Oxford, UK. Google Scholar
  83. E. M McCarthy (2006). Handbook of Avian Hybrids of the World. Oxford University Press, Oxford, UK. Google Scholar
  84. B. D McKayand R. M Zink (2010). The causes of mitochondrial DNA paraphyly in birds. Molecular Phylogenetics and Evolution 54:647–650. Google Scholar
  85. B Milá B. H Warren P Heeband C Thébaud (2010). The geographic scale of diversification on islands: Genetic and morphological divergence at a very small spatial scale in the Mascarene Grey White-eye (Aves: Zosterops borbonicus). BMC Evolutionary Biology 10:158. doi: 10.1186/1471-2148-10-158 Google Scholar
  86. L. S Milesand F. W Allendorf (2002). The one-migrant-per-generation rule in conservation and management. Conservation Biology 10:1509–1519. Google Scholar
  87. H. C Miranda Jr D. S Brooksand R. S Kennedy (2011). Phylogeny and taxonomic review of Philippine lowland scops owls (Strigiformes): Parallel diversification of highland and lowland clades. Wilson Journal of Ornithology 123:441–453. Google Scholar
  88. J. A Moore (1944). Geographic variation in Rana pipiens Schreber of eastern North America. Bulletin of the American Museum of Natural History 82:345–370. Google Scholar
  89. W. S Mooreand J. T Price (1993). Nature of selection in the Northern Flicker hybrid zone and its implications for speciation theory. In Hybrid Zones and the Evolutionary Process ( R. G Harrison Editor). Oxford University Press, Oxford, UK. pp. 196–225. Google Scholar
  90. T. B Mowbray F Cookeand B Ganter (2000). Snow Goose (Chen caerulescens). In The Birds of North America Online ( A Poole Editor). Cornell Lab of Ornithology, Ithaca, NY, USA. doi: 10.2173/bna.514. Google Scholar
  91. S. A Myers S Donnellanand S Kleindorfter (2012). Rainfall can explain adaptive phenotypic variation with high gene flow in the New Holland Honeyeater. Ecology and Evolution 2:2397–2412. Google Scholar
  92. A. G Navarro-Sigüenzaand A. T Peterson (2004). An alternative species taxonomy of the birds of Mexico. Biota Neotropica 4:1–13. Google Scholar
  93. C. E Newman J. A Feinberg L. J Rissler J Burgerand H. B Shaffer (2012). A new species of leopard frog (Anura: Ranidae) from the urban northeastern US. Molecular Phylogenetics and Evolution 63:445–455. doi: 10.1016/j.ympev.2012.01.021 Google Scholar
  94. P Nosil (2012). Ecological Speciation. Oxford University Press, Oxford, UK. Google Scholar
  95. P Nosiland J. L Feder (2013). Genome evolution and speciation: Toward quantitative descriptions of pattern and process. Evolution 67:2461–2467. Google Scholar
  96. P Nosiland D Schluter (2011). The genes underlying the process of speciation. Trends in Ecology and Evolution 26:160–167. Google Scholar
  97. P Nosil T. H Vinesand D. J Funk (2005). Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719. Google Scholar
  98. A. S Nyári (2007). Phylogeographic patterns, molecular and vocal differentiation, and species limits in Schiffornis turdina (Aves). Molecular Phylogeny and Evolution 44:154–164. Google Scholar
  99. R. J O'Hara (1997). Population thinking and tree thinking in systematics. Zoologica Scripta 26:323–329. Google Scholar
  100. A. E Pace (1974). Systematic and biological studies on the leopard frogs (Rana pipiens complex) of the United States. University of Michigan Museum of Zoology Miscellaneous Publications 148. University of Michigan, Ann Arbor, MI, USA. Google Scholar
  101. H. E. H Paterson (1985). The recognition concept of species. In Species and Speciation ( E. S Vrba Editor). Transvaal Museum Monographs No. 4. Transvaal Museum, Pretoria, South Africa. pp. 21–29. Google Scholar
  102. M. A Patten (2010). Null expectations in subspecies diagnosis. Ornithological Monographs 67:35–41. Google Scholar
  103. R. B Payneand M. D Sorenson (2007). Integrative systematics at the species level: Plumage, songs and molecular phylogeny of quailfinches Ortygospiza. Bulletin of the British Ornithological Club 127:4–26. Google Scholar
  104. U Perktas G. F Barrowcloughand J. G Groth (2011). Phylogeography and species limits in the Green Woodpecker complex (Aves: Picidae): Multiple Pleistocene refugia and range expansion across Europe and the Near East. Biological Journal of the Linnean Society 104:710–723. Google Scholar
  105. J. L Peters S. A Sonsthagen P Lavretsky M Rezsutek W. P Johnsonand K. G McCracken (2013). Interspecific hybridization contributes to high genetic diversity and apparent effective population size in an endemic population of Mottled Ducks (Anas fulvigula maculosa). Conservation Genetics. doi: 10.1007/s10592-013-0557-9 Google Scholar
  106. A. T Peterson (2006). Taxonomy is important in conservation: A preliminary reassessment of Philippine species-level bird taxonomy. Bird Conservation International 16:155–173. Google Scholar
  107. A. T Petersonand A. G Navarro-Sigüenza (2006). Consistency of taxonomic treatments: A response to Remsen (2005). The Auk 123:885–887. Google Scholar
  108. A. B Phillimore I. P. F Owens R. A Black J Chittock T Burkeand S. M Clegg (2008). Complex patterns of genetic and phenotypic divergence in an island bird and the consequences for delimiting conservation units. Molecular Ecology 17:2839–2853. Google Scholar
  109. K Popper (2002). The Logic of Scientific Discovery. Routledge, New York, NY, USA. Google Scholar
  110. E Postmaand A. J van Noordwijk (2005). Gene flow maintains a large genetic difference in clutch size at a small spatial scale. Nature 433:65–68. Google Scholar
  111. M Pragerand A. C Wilson (1975). Slow evolutionary loss of the potential for interspecific hybridization in birds: Manifestation of a slow regulatory evolution. Proceedings of the National Academy of Sciences USA 72:200–204. Google Scholar
  112. H. D Pratt (2010). Revisiting species and subspecies of island birds for a better assessment of biodiversity. Ornithological Monographs 67:79–89. Google Scholar
  113. T Price (2008). Speciation in Birds. Roberts and Co., Greenwood Village, CO, USA. Google Scholar
  114. T. D Priceand M. M Bouvier (2002). The evolution of F1 postzygotic incompatibilities in birds. Evolution 56:2083–2089. Google Scholar
  115. R. O Prum (2010). The Lande-Kirkpatrick mechanism is the null model of evolution by intersexual selection: Implications for meaning, honesty, and design in intersexual signals. Evolution 64:3085–3100. Google Scholar
  116. D. L Raboskyand D. R Matute (2013). Macroevolutionary speciation rates are decoupled from the evolution of intrinsic reproductive isolation in Drosophila and birds. Proceedings of the National Academy of Sciences USA 110:15354–15359. Google Scholar
  117. P. C Rasmussen D. N. S Allen N. J Collar B DeMeulemeester R. O Hutchinson P. G. C Jakosalem R. S Kennedy F. R Lambertand L. M Paguntalan (2012). Vocal divergence and new species in the Philippine Hawk Owl Ninox philippensis complex. Forktail 28:1–20. Google Scholar
  118. S Reddy (2008). Systematics and biogeography of the shrike-babblers (Pteruthius): Species limits, molecular phylogenetics, and diversification patterns across southern Asia. Molecular Phylogenetics and Evolution 47:54–72. Google Scholar
  119. N Reidand B Carstens (2012). Phylogenetic estimation error can decrease the accuracy of species delimitation: A Bayesian implementation of the general mixed Yule-coalescent model. BMC Evolutionary Biology 12:196. doi: 10.1186/1471-2148-12-196 Google Scholar
  120. J. V Remsen Jr (2005). Pattern, process, and rigor meet classification. The Auk 122:403–413. Google Scholar
  121. J. V Remsen Jr (2010). Subspecies as a meaningful taxonomic rank in avian classification. Ornithological Monographs 67:62–78. Google Scholar
  122. J. V Remsen Jr (Editor) (2013). A classification of the bird species of South America. American Ornithologists' Union.∼Remsen/SACCBaseline.html Google Scholar
  123. F. E Rheindtand J. A Eaton (2009). Species limits in Pteruthius (Aves: Corvida) shrike-babblers: A comparison between the biological and phylogenetic species concepts. Zootaxa 2301:29–54. Google Scholar
  124. F. E Rheindtand S. V Edwards (2011). Genetic introgression: An integral but neglected component of speciation in birds. The Auk 128:620–632. Google Scholar
  125. J. M Rhymerand D Simberloff (1996). Extinction by hybridization and introgression. Annual Review of Ecology and Systematics 27:83–109. Google Scholar
  126. J. M Rhymer M. J Williamsand M. J Braun (1994). MtDNA gene flow between Grey Ducks and Mallards in New Zealand. The Auk 111:970–978. Google Scholar
  127. A. M Ribeiro P Lloydand R. C. K Bowie (2011). A tight balance between natural selection and gene flow in a southern African arid-zone endemic bird. Evolution 65:3499–3514. Google Scholar
  128. R. E Ricklefs (2005). Taxon cycles: Insights from invasive species. In Species Invasions: Insights into Ecology, Evolution, and Biogeography ( D. F Sax J. J Stachowiczand S. D Gaines Editors). Sinauer Associates, Sunderland, MA, USA. pp. 165–199. Google Scholar
  129. S Rohwer E Berminghamand C Wood (2001). Plumage and mitochondrial DNA haplotype variation across a moving hybrid zone. Evolution 55:405–422. Google Scholar
  130. O. R Rojas-Soto A. G Navarro-Siqüenzaand A Espinosa de los Monteros (2010). Systematics and bird conservation policies: The importance of species limits. Bird Conservation International 20:176–185. doi: 10.1017/S0959270909990268 Google Scholar
  131. L. A Sánchez-Gonzálezand R. G Moyle (2011). Molecular systematics and species limits in the Philippine fantails (Aves: Rhipidura). Molecular Phylogeny and Evolution 61:290–299. Google Scholar
  132. G Sangster (2009). Increasing numbers of bird species result from taxonomic progress, not taxonomic inflation. Proceedings of the Royal Society B 276:3185–3191. Google Scholar
  133. G Sangster (2013). The application of species criteria in avian taxonomy and its implications for the debate over species concepts. Biological Reviews. doi: 10.1111/brv.12051 Google Scholar
  134. D Schluter (2009). Evidence for ecological speciation and its alternative. Science 323:737–741. Google Scholar
  135. N Seddon C. A Botero J. A Tobias P. O Dunn H. E. A MacGregor D. R Rubenstein J. A. C Uy J. T Weir L. A Whittinghamand R. J Safran (2013). Sexual selection accelerates signal evolution during speciation in birds. Proceedings Royal Society B 280, no. 1766. doi: 10.1098/rspb.2013.106542 Google Scholar
  136. G Seutin J Brawn R. E Ricklefsand E Bermingham (1993). Genetic divergence among populations of a tropical passerine, the Streaked Saltator (Saltator albicollis). The Auk 110:117–126. Google Scholar
  137. R. B Sharpe (1909). A Hand-list of the Genera and Species of Birds. Volume 5. British Museum (Natural History), London, UK. Google Scholar
  138. N. D Sly A. K Townsend C. C Rimmer J. M Townsend S. C Lattaand I. J Lovette (2011). Ancient islands and modern invasions: Disparate phylogeographic histories among Hispaniola's endemic birds. Molecular Ecology 20:5012–5024. Google Scholar
  139. A. R Templeton (2008). The reality and importance of founder speciation in evolution. BioEssays 30:470–479. Google Scholar
  140. J. A Tobias J. M Bates S. J Hackettand N Seddon (2008). Comment on “The latitudinal gradient in recent speciation and extinction rates of birds and mammals.” Science 319:901. doi: 10.1126/science.1150568 Google Scholar
  141. J. A Tobias N Seddon C. N Spottiswoode J. D Pilgrim L. D. C Fishpooland N. J Collar (2010). Quantitative criteria for species delimitation. Ibis 152:724–746. Google Scholar
  142. D. P. L Toews M Mandic J. G Richardsand D. E Irwin (2013). Migration, mitochondria and the Yellow-rumped Warbler. Evolution OnLine. doi: 10.1111/evo.12260 Google Scholar
  143. P. L Tubaroand D. A Lijtmaer (2002). Hybridization patterns and the evolution of reproductive isolation in ducks. Biological Journal of the Linnean Society 77:193–200. Google Scholar
  144. C Uy J. T Weir L. A Whittinghamand R. J Safran (2013). Sexual selection accelerates signal evolution during speciation in birds. Proceedings of the Royal Society B 280:20131065. doi: 10.1098/rspb.2013.1065 Google Scholar
  145. R Vallender R. J Robertson V. L Friesenand I. J Lovette (2007). Complex hybridization dynamics between Golden-winged and Blue-winged Warblers (Vermivora chrysoptera and Vermivora pinus) revealed by AFLP, microsatellite, intron and mtDNA markers. Molecular Ecology 16:2017–2029. Google Scholar
  146. E. A VanderWerf (2012). Ecogeographic patterns of morphological variation in elepaios (Chasiempis spp.): Bergmann's, Allen's, and Gloger's Rules in a microcosm. Ornithological Monographs 73:1–34. Google Scholar
  147. J Wakeley (2008). Coalescent Theory: An Introduction. Roberts and Company Publishers, Greenwood Village, CO, USA. Google Scholar
  148. J Wakeley (2010). Natural selection and coalescent theory. In Evolution since Darwin: The First 150 Years ( M. A Bell D. J Futuyma W. F Eanesand J. S Levinton Editors). Sinauer and Associates, Sunderland, MA, USA. pp. 119–149. Google Scholar
  149. H. E Walsh I. L Jonesand V. L Friesen (2005). A test of founder effect speciation using multiple loci in the auklets (Aethia spp.). Genetics 171:1885–1894. Google Scholar
  150. J. C Weckstein R. M Zink R. C Blackwell-Ragoand D. A Nelson (2001). Anomalous variation in mitochondrial genomes of White-crowned (Zonotrichia leucophrys) and Golden-crowned (Z. atricapilla) Sparrows: Pseudogenes, hybridization, or incomplete lineage sorting? The Auk 118:231–236. Google Scholar
  151. K. L Wiebe (2000). Assortative mating by color in a population of hybrid Northern Flickers. The Auk 117:525–529. Google Scholar
  152. M Williamsand B Basse (2006). Indigenous Gray Ducks, Anas superciliosa, and introduced Mallards, A. platyrhynchos, in New Zealand: Processes and outcome of a deliberate encounter. Acta Zoologica Sinica 52(Supplement):579–582. Google Scholar
  153. K Winker (2010). Is it a species? Ibis 152:679–682. Google Scholar
  154. K Winker K. G McCracken D. D Gibsonand J. L Peters (2013). Heteropatric speciation in a duck, Anas crecca. Molecular Ecology 22:5922–5935. Google Scholar
  155. J. B. W Wolf J Lindelland N Backström (2010). Speciation genetics: Current status and evolving approaches. Philosphical Transactions of the Royal Society B 365:1717–1733. Google Scholar
  156. N. A Wrightand D. W Steadman (2012). Insular avian adaptations on two Neotropical continental islands. Journal of Biogeography 39:1891–1899. doi: 10.1111/j.1365–2699.2012.02754.x Google Scholar
  157. Z Yangand B Rannala (2010). Bayesian species delimitation using multilocus sequence data. Proceedings of the National Academy of Sciences USA 107:9264–9269. Google Scholar
  158. R. M Zink (1996). Species concepts, speciation, and sexual selection. Journal of Avian Biology 27:1–6. Google Scholar
  159. R. M Zink (1997). Phylogeographic studies of North American birds. In Avian Molecular Evolution and Systematics ( D Mindell Editor). Academic Press, San Diego, CA, USA. pp 301–324. Google Scholar
  160. R. M Zink (2006). Rigor and species concepts. The Auk 123:887–891. Google Scholar
  161. R. M Zinkand G. F Barrowclough (2008). Mitochondrial DNA under siege in avian phylogeography. Molecular Ecology 17:2107–2121. Google Scholar
  162. R. M Zinkand M. C McKitrick (1995). The debate over species concepts and its implications for ornithology. The Auk 112:701–719. Google Scholar
and Frank B. Gill "Species taxonomy of birds: Which null hypothesis?," The Auk 131(2), (5 March 2014).
Received: 26 October 2013; Accepted: 1 December 2013; Published: 5 March 2014

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