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Kristen C. Ruegg, Michaela Brinkmeyer, Christen M. Bossu, Rachael A. Bay, Eric C. Anderson, Clint W. Boal, Russell D. Dawson, Amber Eschenbauch, Christopher J. W. McClure, Karl E. Miller, Lance Morrow, Jill Morrow, M. David Oleyar, Bill Ralph, Sarah Schulwitz, Ted Swem, Jean-Francois Therrien, Rich Van Buskirk, Thomas B. Smith, Julie A. Heath
Identifying population genetic structure is useful for inferring evolutionary process and comparing the resulting structure with subspecies boundaries can aid in species management. The American Kestrel (Falco sparverius) is a widespread and highly diverse species with 17 total subspecies, only 2 of which are found north of U.S./Mexico border (F. s. paulus is restricted to southeastern United States, while F. s. sparverius breeds across the remainder of the U.S. and Canadian distribution). In many parts of their U.S. and Canadian range, American Kestrels have been declining, but it has been difficult to interpret demographic trends without a clearer understanding of gene flow among populations. Here we sequence the first American Kestrel genome and scan the genome of 197 individuals from 12 sampling locations across the United States and Canada in order to identify population structure. To validate signatures of population structure and fill in sampling gaps across the U.S. and Canadian range, we screened 192 outlier loci in an additional 376 samples from 34 sampling locations. Overall, our analyses support the existence of 5 genetically distinct populations of American Kestrels—eastern, western, Texas, Florida, and Alaska. Interestingly, we found that while our genome-wide genetic data support the existence of previously described subspecies boundaries in the United States and Canada, genetic differences across the sampled range correlate more with putative migratory phenotypes (resident, long-distance, and short-distance migrants) rather than a priori described subspecies boundaries per se. Based on our results, we suggest the resulting 5 genetically distinct populations serve as the foundation for American Kestrel conservation and management in the face of future threats.
LAY SUMMARY
The American Kestrel (Falco sparverius) is a widespread iconic raptor species that has shown highly variable trends in abundance over the last several decades.
Here we sequence the first American Kestrel genome and scan the genome for genetic variation in order to identify five genetically distinct populations across the U.S. and Canadian breeding range.
The resulting map of genetic variation (the genoscape) can serve as a foundation for testing hypotheses to explain observed population-specific responses to climate change and other stressors.
Given the availability of genomic data to identify separately evolving groups of organisms, many researchers establish species limits based on assessments of the extent of gene flow among populations and often use analytical approaches to identify species in which gene flow is explicitly disallowed. Strictly considering lack of—or limited—gene flow as the main or only criterion to delimit species involves two main complications in practice. First, approaches often used to analyze genome-wide data cannot by themselves distinguish species limits from within-species population structure, particularly in allopatric organisms. Second, recognizing as species only those lineages one can identify using such approaches fails to embrace the role of other evolutionary forces (i.e. various forms of selection) in defining evolutionary lineages. Using examples from various groups of birds, we call for the importance of considering evolutionary forces additional to gene flow in species delimitation and explain why genomic approaches commonly used in taxonomic studies may be insufficient by themselves to properly uncover species limits. By considering the processes that structure genotypic and phenotypic variation during speciation, we argue that rigorous analyses of phenotypic variation remain crucial for species delimitation in the genomics era because phenotypes uniquely inform us about the role of selection maintaining the cohesion of evolutionary lineages. Evolutionary theory describing the roles of gene flow, genetic drift and natural and sexual selection in the origin and maintenance of species calls for an integration of genomics with phenomics in avian species delimitation.
LAY SUMMARY
State-of-the-art approaches to delimit bird species using genomic data do not properly account for all the evolutionary forces that generate avian diversity.
A dominant paradigm followed by ornithologists to delimit bird species relies on inferences of reproductive isolation between populations.
We review evidence from genetic and genomic studies in avian taxonomy and show these have significant limitations because many species are less reproductively isolated (i.e. exchange more genes) than previously thought.
We argue that studies using phenotypic data and methods properly grounded on evolutionary theory offer unique insight to delimit species because they shed light on the role of selection in generating and maintaining biodiversity.
Because species play a central role in biology, delimiting species using genomic and phenotypic data on equal footing is necessary to effectively capture the reality of species as the products of evolution.
Africa's montane ecosystems are noteworthy not only for their isolation but for their morphologically similar bird populations that inhabit geographically disparate localities. Many species possess range disjunctions in excess of 2,000 km and appear to represent populations that have been isolated since at least the last Ice Age, including the Northern Double-collared Sunbird (Cinnyris reichenowi). Recent work on other Afromontane birds has demonstrated substantial phylogeographic structure can exist in phenotypically similar populations, with cryptic species occurring parapatrically within the same mountain range. We explored genetic, morphological, and ecological diversity within C. reichenowi to assess whether cryptic regional diversification occurs across the disjunct portions of this species' range. Within C. reichenowi, we find consistent patterns of morphological disparity that coincide with genetic diversification between xeric and wet montane populations within the Cameroon Line in the Western population, and clear genetic differentiation between Western and Eastern populations. Our research demonstrates that the geographically isolated populations of C. reichenowi represent different species, and that ecological diversification is shaping populations within Central Africa. We show here that two named populations should be recognized as members of a western species in the Northern Double-collared Sunbird complex: nominate Cinnyris preussi preussi in the Cameroon Line montane forests, and Cinnyris preussi genderuensis in the more xeric interior of Cameroon and the Central African Republic, likely occurring in adjacent Nigeria as well.
LAY SUMMARY
Northern Double-collared Sunbirds (Cinnyris reichenowi) look similar across their range, but they have a complicated taxonomic history and inhabit a wide range of habitats.
Combining genetics, morphology, and ecology, we uncovered surprising patterns of diversification, resurrecting a defunct taxon (subspecies genderuensis) while shedding light on diversification processes.
Our results show a clear separation between eastern and western populations, and ongoing diversification occurring between adjacent western groups.
This work furthers our knowledge of Afromontane diversification patterns, finding three differentiable groups within the Northern Double-collared Sunbird.
KEYWORDS: body condition, Bubo scandiacus, Global positioning system/Global system for mobile communication, land cover composition, movement pattern, nonbreeding, wintering areas
Migrating animals occur along a continuum from species that spend the nonbreeding season at a fixed location to species that are nomadic during the nonbreeding season, essentially continuously moving. Such variation is likely driven by the economics of territoriality or heterogeneity in the environment. The Snowy Owl (Bubo scandiacus) is known for its complex seasonal movements, and thus an excellent model to test these ideas, as many individuals travel unpredictably along irregular routes during both the breeding and nonbreeding seasons. Two possible explanations for this large variation in the propensity to move are (1) dominance hierarchies in which dominant individuals (adult females in this case) monopolize some key, consistent resources, and move less than subdominants; and (2) habitat heterogeneity in which individuals foraging in rich and less heterogenic environments are less mobile. We analyzed fine-scale telemetry data (global positioning system [GPS]/global system for mobile communication [GSM]) from 50 Snowy Owls tagged in eastern and central North America from 2013 to 2019, comparing space use during the winter period according to sex and age, and to land cover attributes. We used variograms to classify individuals as nomadic (58%) or range-resident (42%), and found that nomadic owls had ten times larger wintering areas than range-resident owls. The frequency of nomadism was similar in socially-dominant adult females, immatures, and males. However, nomadism increased from west to east, and north to south, and was positively associated with the use of water and negatively associated with croplands. We conclude that many individual Snowy Owls in Eastern North America are nomadic during the nonbreeding season and that movement patterns during this time are driven primarily by extrinsic factors, specifically heterogeneity in habitat and prey availability, as opposed to intrinsic factors associated with spacing behavior, such as age and sex.
LAY SUMMARY
Global positioning system (GPS)/Global system for mobile communication (GSM) transmitters were used to document two movement behaviors, range-residency, and nomadism in wintering Snowy Owls.
Social dominance plays little role in determining the distribution of wintering owls in temperate areas.
Mobility increased west to east, and north to south, and was more common along with bodies of water than in croplands.
Rainfall regime, the amount and timing of annual precipitation, can influence the breeding phenology, individual fitness, and population dynamics of tropical birds. In Neotropical regions with rainfall seasonality (i.e. wet and dry seasons), the warm phase of the El Niño Southern Oscillation (ENSO) can exacerbate seasonal drought and negatively impact avian survival and reproduction. However, the mechanisms underlying associations between seasonal drought conditions and avian demography are largely unexplored. One hypothesis is that nutritional condition mediates demographic responses to seasonal drought: individuals in poor condition may be less capable of balancing their energy budgets and consequently suffer reduced survival, lower reproductive output, or both. We estimated nutritional condition (i.e. scaled mass index, percent hematocrit, plasma lipid metabolites) as a proxy of energy balance in understory forest birds with contrasting population-level responses to dry season length. This study took place across two dry seasons of differing intensity in central Panama: an El Niño dry season (2016, severe drought) and a more typical dry season (2017). Scaled mass index remained relatively constant throughout both dry seasons and across years for 5 common focal species and among 4 foraging guilds (22 additional species, 27 species total). Three of 5 focal species did exhibit reduced nutritional condition (i.e. lower hematocrit and/or higher β-hydroxybutyrate) during the El Niño dry season but not during the more typical dry season. However, foraging guilds did not show consistent nutritional responses to seasonal drought and we found little evidence of the reduced nutritional condition at the guild level, suggesting that many Neotropical forest bird species are capable of tolerating seasonal drought.
LAY SUMMARY
The amount and timing of rainfall influences the ecology, phenology, and population dynamics of tropical organisms.
Seasonal drought can negatively impact the survival, reproduction, and breeding phenology of tropical forest birds, although the mechanisms underlying these impacts remain unclear.
We tested the hypothesis that seasonal drought negatively impacts the nutritional condition of resident forest birds in Central Panama.
We estimated body condition, hematocrit, and plasma lipid metabolite concentrations in 27 bird species across two dry seasons of differing intensity—an El Niño year (2016, very dry) and a more typical year (2017).
We found some evidence of reduced nutritional condition (i.e. lower hematocrit and greater concentrations of β-hydroxybutyrate) during the El Niño dry season in certain focal species, but little evidence of nutritional stress among foraging guilds.
Our findings suggest that many tropical forest species can tolerate seasonal drought without exhibiting evidence of energetic stress.
Habitat selection decisions can impact individual fitness and ultimately scale up to mediate population dynamics. Understanding how birds select habitat is thus critical for discerning the biological processes structuring populations and for developing conservation strategies, particularly for species in decline. Marbled Murrelet (Brachyramphus marmoratus; hereafter murrelet) populations have declined in recent decades due to loss of late-successional forest nesting habitat and changing ocean conditions that impact foraging success. Most other seabirds in the family Alcidae nest colonially and evidence suggests nesting murrelets may aggregate in stands, yet no studies have examined murrelet use of social information in nest-site selection. In 2016, we experimentally simulated the presence of murrelets at 14 randomly chosen potential breeding sites by broadcasting murrelet calls throughout the breeding period. Between broadcasting bouts, we recorded calls of wild murrelets and compared call rates with those recorded at 14 control sites (no broadcast). One year after playbacks ceased (2017) we conducted breeding season surveys to document behaviors indicative of murrelet breeding activity. Broadcasting murrelet calls in 2016 increased daily odds of wild murrelets vocalizing during the treatment period by up to 15.4× (95% CI: 2.3, 125.4) relative to control sites. During the 2017 breeding season, the odds of occupancy were 10.0× (CI: 1.2, 81.4) greater at treatment sites than control sites. These results indicate that social information influences murrelet breeding site selection because the simulated conspecific presence in potential nesting habitat appeared to attract prospectors in 2016 that continued occupying treatment sites the following year. This conspecific attraction implies murrelet nesting sites are likely to remain occupied over time and that large tracts of nesting habitat may be important for supporting murrelet populations. Murrelets may also be susceptible to information-mediated Allee effects whereby a lack of conspecific information about nesting habitat could exacerbate long-term population declines.
LAY SUMMARY
We found that Marbled Murrelets are attracted to potential breeding areas based on the presence of other Marbled Murrelets.
The odds of murrelets occupying sites where we previously broadcast murrelet calls were about 10 times greater than at sites where we did not play calls.
Murrelet populations have been declining, and recovery may be hindered by the fact that there are few murrelets available to provide information to others about where to nest.
Managers could consider broadcasting vocalizations to encourage murrelets to nest in unused, high-quality habitat.
Because murrelets are attracted to other murrelets, protecting areas adjacent to known nesting sites may also be an effective conservation approach.
Elevational migration can be defined as roundtrip seasonal movement that involves upward and downward shifts in elevation. These shifts incur physiological challenges that are proportional to the degree of elevational change. Larger shifts in elevation correspond to larger shifts in partial pressure of oxygen, air density, temperature, and ultraviolet (UV) exposure. Although most avian examples of elevational migration involve subtle shifts that would have minimal impacts on physiology, shifts of any magnitude have previously been considered under the broad umbrella of “elevational migration”. Here, we consider extreme seasonal elevational movements (≥2,000 m), sufficient to shift the elevational dimension of the eco-climatic niche. Migratory bird populations typically maintain inter-seasonal stability in the temperature, precipitation, and elevational aspects of their climatic niches, a tendency that likely reflects genetic physiological specialization on environmental conditions such as atmospheric pressure. A shift of ≥2,000 m involves a ≥20% change in air density and oxygen partial pressure, sufficient to incur functionally impactful declines in arterial blood-oxygen saturation and require compensatory shifts in respiratory physiology. We refer to this phenomenon as elevational niche-shift migration (ENSM). In this review, we analyzed >4 million occurrence records to identify 105 populations, representing 92 bird species, that undergo complete or partial ENSM. We identified key ecological and evolutionary questions regarding the causes and consequences of ENSM. Our synthesis reveals that ENSM has evolved independently in at least 29 avian families spanning 10 orders. Nonetheless, ENSM is rare relative to other forms of seasonal migration, consistent with the general tendency of seasonal niche conservatism by migratory species and evolutionarily conserved elevational range limits. For many migratory species and populations, within-species patterns of migratory connectivity are not sufficiently understood to determine ENSM status. ENSM is distinguished by its scale within the broader phenomenon of elevational migration. Critical examination of ENSM illustrates fundamental constraints on the ecology and evolution of migration systems, topographical influences on geographic patterns of migratory connectivity, and the remarkable metabolic flexibility of certain bird species that allows them to occupy disparate elevations across different seasons.
LAY SUMMARY
Migratory birds that make extreme elevational movements between breeding and nonbreeding seasons cope with many challenges, including fluctuating oxygen availability.
We call this phenomenon “elevational niche-shift migration” (ENSM), because large seasonal elevational shift (≥2,000 m) are accompanied by large shifts in ecological and climatic conditions that define a species' niche.
We analyzed >4 million occurrence records and searched the literature to identify the subset of migratory birds that undergo ENSM: 105 populations, representing 92 species, 29 families, and 10 orders.
ENSM has evolved >100 times across the avian tree, with most instances in the Himalayas and the Andes. Songbirds comprise >75% of ENSM populations. More than 90% of ENSM populations breed high, migrating to nonbreeding grounds at lower elevations.
ENSM exemplifies a striking seasonal niche shift, whereby birds use phenotypic flexibility to maintain performance under vastly different atmospheric pressures, while exhibiting traits typically associated with high-altitude species.
Although primary cavity-nesting species are capable of excavating new cavities, they often reuse old ones. To determine potential factors driving such reuse, we studied nest-cavity reuse in the Acorn Woodpecker (Melanerpes formicivorus), a cooperatively breeding species that reuses old cavities for 57.2% of nests at Hastings Reservation in central coastal California, USA. We found no evidence for significant fitness costs or benefits of cavity reuse compared to using newly constructed cavities. In contrast, several lines of evidence supported a role for constraints on both cavity reuse and on new cavity construction. The main constraint on reuse was cavities failing to survive from one year to the next, usually because the limb fell apart, filled with water, or was usurped by another species. Evidence that constraints on new cavity construction may be important included more frequent cavity reuse when groups renested and use of artificial cavities when they were experimentally provided. Nest-cavity reuse in this population appears to be driven primarily by constraints, including the energetic costs and time required to excavate a new cavity, rather than fitness consequences, even though Acorn Woodpeckers regularly excavate small holes in trees for acorn storage and the energetic costs of new cavity construction are apparently insufficient to significantly depress reproductive success. Constraints play a significant role in cavity reuse and may affect both the intraspecific and interspecific frequency of cavity reuse among facultative excavating species.
LAY SUMMARY
We investigated the costs and benefits of cavity reuse in the cooperatively breeding Acorn Woodpecker (Melanerpes formicivorus), in which groups reuse old cavities for over half of nesting attempts.
We found no differences in the fledgling success of family groups that reused an old cavity compared to excavating a new one. Why, then, do birds reuse old cavities?
The answer appears to be constraints, both on cavity reuse and new cavity construction.
The main constraint on cavity reuse was that many cavities become unusable from one year to the next, usually because the tree limb disintegrates, fills with water, or is taken over by another species.
Birds frequently use artificial cavities when they are provided, suggesting that old cavities are reused because excavating a new one takes time and energy.
Constraints appear to play a significant role in cavity reuse and may affect both the frequency of cavity reuse among species and across populations of excavating species.
Understanding the evolutionary and ecological mechanisms that shape the spatial divergence of signals involved in reproductive isolation is a central goal in studies of speciation. For birds with innate songs, such as the suboscine passerine birds, the integration and comparison of both genetic and ecological factors in explaining song variation at the microevolutionary scale are rare. Here, we evaluated the evolutionary and ecological processes underlying the variation in the songs of the Atlantic Forest endemic Drab-breasted Bamboo Tyrant (Hemitriccus diops), testing the effects of both stochastic and adaptive processes, namely the stochastic and acoustic adaptation hypotheses, respectively. We combined vocal, genetic, and ecological (climate and forest cover) data across the species' range. To this end, we analyzed 89 samples of long and short songs. We performed analyses on raw and synthetic data song variables with linear mixed models and multivariate statistics. Our results show that both song types differ in spectral features between the 2 extant phylogeographic lineages of this species, but such vocal divergence is weak and subtle in both song types. Overall, there is a positive relationship of acoustic distances with the amount of forest cover in long songs. Our results suggest that there is cryptic geographical variation in both song types and that this variation is associated with low levels of genetic divergence in both songs and with ecological factors in long songs.
LAY SUMMARY
Birds with innate songs constitute good models to evaluate the role of ecological and evolutionary forces in shaping vocal geographic variation.
Here, we tested if selective and stochastic–neutral factors underlay the spatial variation in two types of songs in a Neotropical suboscine bird.
To this end, we contrasted the variation in songs with genetic and environmental variation across the entire species range.
We found that there is cryptic geographical variation in both song types and that this variation is associated with low levels of genetic divergence in both songs and with ecological factors in long songs.
Examining differences among recently diverged populations can provide insight into the traits and evolutionary mechanisms that drive or maintain divergence. The genus Sturnella includes 2 recently diverged species, Sturnella magna (Eastern Meadowlark) and S. neglecta (Western Meadowlark), the former of which has a complex of subspecies distributed across the Americas. Of the S. magna subspecies that occur in the United States, S. m. lilianae is the only one with a disjunct range, occurring in the southwestern United States and central Mexico. It also has markedly different song patterns than all other S. magna subspecies. In order to assess population differentiation, we performed whole-genome sequencing of 35 birds and analyzed song characteristics from 85 birds. Songs from each species and S. m. lilianae were diagnosable using linear discriminant function analysis and support divergence in song between all taxa. Phylogenetic analysis and admixture proportions support 3 distinct clades within North American meadowlarks, and tests of introgression failed to detect a significant signal. Overall, our results indicate that S. m. lilianae exhibits high levels of genetic and vocal differentiation from both S. magna and S. neglecta, with no evidence of introgression between any group, and forms a distinct evolutionary lineage. We thus recommend the elevation of S. m. lilianae to species status.
LAY SUMMARY
• Understanding species boundaries helps inform policy.
• Meadowlarks are currently classified as two species, but recent research suggests they may be three species.
• A population of Eastern Meadowlarks in the southwestern United States and northern Mexico called Lilian's Meadowlark have lighter plumage color and sing different songs than the rest of Eastern Meadowlarks.
• Using DNA and birdsong, we compared populations of Eastern, Western, and Lilian's meadowlarks to find how they were related to one another.
• Eastern, Western, and Lilian's meadowlarks all have moderate but equal amounts of differentiation from one another, suggesting Lilian's Meadowlarks is a full species.
Accurately determining avian species limits has been a challenge and a work in progress for most of a century. It is a fascinating but difficult problem. Under the biological species concept, only lineages that remain essentially independent when they are in sympatry are clearly species. Otherwise, there is no clear line yet found that marks when a pair of diverging lineages (e.g., in allopatry) become different enough to warrant full biological species status. Also, with more data, species limits often require reevaluation. The process of divergence and speciation is itself very complex and is the focus of intense research. Translating what we understand of that process into taxonomic names can be challenging. A series of issues are important. Single-locus criteria are unlikely to be convincing. Genetic independence is not a species limits requirement, but the degree of independence (gene flow) needs to be considered when there is opportunity for gene flow and independence is not complete. Time-based species (limits determined by time of separation) are unsatisfactory, though integrating time more effectively into our datasets is warranted. We need to disentangle data signal due to neutral processes vs. selection and prioritize the latter as the main driver of speciation. Assortative mating is also not likely to be an adequate criterion for determining species limits. Hybridization and gene flow are more important than ever, and there is a condition not being treated evenly in taxonomy: evolutionary trysts of 2 or more lineages stuck together through gene flow just short of speciation over long periods. Comparative methods that use what occurs between good species in contact to infer species limits among allopatric forms remain the gold standard, but they can be inaccurate and controversial. Species-level taxonomy in birds is likely to remain unsettled for some time. While the study of avian speciation has never been more exciting and dynamic, there is no silver bullet for species delimitation, nor is it likely that there will ever be one. Careful work using integrative taxonomy in a comparative framework is the most promising way forward.
LAY SUMMARY
The process of population divergence and speciation produces avian diversity but is very complex.
I review this process and some of the challenges we have in translating this knowledge into taxonomic names.
Natural and sexual selection, gene flow, time, and neutral changes affect lineages differently, creating difficult puzzles for us to solve when asking “Is it a species?”
Avian taxonomy will continue to change as we improve our data and analyses and test historic hypotheses about species limits.
An integrative approach using diverse datasets in a comparative framework is the most promising way forward.
Sex allocation theory predicts that parents should adjust their brood sex ratio to maximize fitness returns in relation to parental investment. Adaptive adjustment of sex ratio may be driven by differential costs of rearing sons and daughters or differential benefits of investing limited resources into offspring of different sex. In both cases, possible sex ratio bias should depend on parental condition. For sexually dimorphic birds with males larger than females, sons may be less likely to fledge since they are more vulnerable to food shortages or because they have impaired immunocompetence due to higher testosterone levels. Poor condition females should thus overproduce daughters to minimize possible reproductive failure. We manipulated the number of eggs laid and the amount of food available to laying females to induce differences in the condition in 2 gull species differing in sexual size dimorphism. In the Black-headed Gull (Chroicocephalus ridibundus), sexual size differences are marginal; but in the Mew Gull (Larus canus), males are 11% larger. In both species, females forced to lay an additional egg (presumed in worse condition) overproduced daughters, whereas females receiving supplemental food before laying (presumed improved condition) overproduced sons. This sex ratio skew was larger in Mew Gull, a species with larger size dimorphism. Chick immunocompetence at hatching was unrelated to sex, being higher in broods of fed mothers and lower for chicks hatched from last-laid eggs. Chick survival between hatching and day 5 post-hatch was positively related to their immunocompetence, but chicks from last-laid eggs and males of Mew Gull, the more dimorphic species, survived less well. Results indicate that costs of raising larger sex offspring coupled with parental condition shape brood sex ratio in populations studied. Adaptive brood sex ratio adjustment occurs mostly before egg laying and includes differential sex allocation in eggs depending on the probability of producing a fledged chick.
LAY SUMMARY
We found that Mew Gull and Black-headed Gull change the proportion of sons and daughters in their broods depending on the parental condition during egg laying. Natural selection should favor deviations from parity of sexes among offspring if the costs or benefits of producing sons and daughters are different.
We tested this by manipulating the condition of gulls before egg laying and found that in both species females in poor condition had more daughters whereas females receiving extra food had more sons.
These differences were larger in the species where males are 11% heavier than females (i.e. Mew Gull) than in species where both sexes are of similar size (i.e. Black-headed Gull).
It shows that differential costs of raising sexes shape the brood sex ratio in addition to parental condition.
Additionally, improved parental condition translated into improved immunocompetence of chicks, which enhanced their chances of surviving the first days of life irrespective of sex.
Species delimitation requires a broad assessment of population-level variation using multiple lines of evidence, a process known as integrative taxonomy. More specifically, studies of species limits must address underlying questions of what limits the distribution of populations, how traits vary in association with different environments, and whether the observed trait differences may lead to speciation through reproductive isolation. While genomic data have revolutionized the process of delimiting species, such data should be analyzed along with phenotypic, behavioral, and ecological traits that shape individuals across geographic and environmental space. The integration of multiple traits promotes taxonomic stability and should be a major guiding principle for species delimitation. Equally important, however, is thorough geographic sampling to adequately represent population-level variation—both in allopatry and across putative contact zones. We discuss the importance of both of these factors in the context of species concepts and traits and present different examples from birds that illustrate criteria for species delimitation. In addition, we review a decade of proposals for species-level taxonomic revisions considered by the American Ornithological Society's North American Classification Committee, and summarize the basis for decisions on whether to split or lump species. Finally, we present recommendations and discuss challenges (specifically permits, time, and funding) for species delimitation studies. This is an exciting time to be studying species delimitation in birds: many species-level questions remain, and methodological advances along with increased access to data enable new approaches to studying age-old problems in avian taxonomy.
LAY SUMMARY
Standardized taxonomy and nomenclature are fundamental to biodiversity research and conservation, with wide-reaching impacts for diverse stakeholders.
Rigorous approaches to species delimitation require an integrative assessment of population-level variation using multiple lines of evidence and robust geographic sampling.
Sampling should reflect phenotypic, ecological, and behavioral trait variation and include contact zones between divergent populations if relevant.
We review basic concepts and criteria in species delimitation, drawing from examples across different avian lineages.
We summarize the outcomes of a decade of species-level proposals considered by the American Ornithological Society's North American Classification Committee.
We provide recommendations and discuss challenges for researchers interested in pursuing species-level taxonomic studies.
Many species-level questions remain in ornithology, and this is an exciting time to be studying integrative species delimitation in birds.
The ornithological world has 4 global checklists (as of early 2020). While 3 follow the results of peer-reviewed research at varying pace and conservatism, the HBW/BirdLife checklist, which is adopted by the global Red List authority, has implemented Tobias et al.'s (2010) 7-point scoring system to overhaul global ornithological treatment. Critically received in some academic quarters, this scoring system is lauded by other ornithologists for its simplicity and reproducibility, a claim that remains to be tested. We subjected 26 ornithologists to a set of 48 bird skins belonging to 20 controversial taxonomic complexes and observed a wide variance in scoring results, in most cases straddling anywhere from far below to above the species threshold of the 7-point rule and casting doubt on claims of high reproducibility. For a detailed assessment of genuine taxonomic discord, we compared the taxonomic coverage of the avifauna of the Indonesian Archipelago (comprising ∼1,400 species) between the HBW/BirdLife checklist, other major authorities, and the peer-reviewed literature. We detected that controversial treatments supported by the 7-point rule but at odds with the peer-reviewed literature predominantly refer to lumps, not splits, which are the usual subject of modern taxonomic quarrels. Notably, the method tends to unite morphologically (and sometimes vocally) cryptic forms into single larger species because of its inability to accommodate molecular and massive bioacoustic datasets that would indicate otherwise. On the other hand, the 7-point rule has produced numerous novel proposals for splits that may or may not be corroborated by future peer-reviewed inquiry. We recommend the 7-point rule as one of the multiple unofficial exploratory tools to flag cases of potentially cryptic species requiring further inquiry, but we advise against its adoption by other taxonomic authorities and the ornithological community.
LAY SUMMARY
Competing authorities continue to be in ample disagreement about birds' classification.
The checklist that Birdlife International applies to the global Red List is unique in that a standardized scoring system, the 7-point rule, was adopted to overhaul taxonomic treatments, often overturning the results of peer-reviewed research.
We explored the magnitude of conflict generated by application of the 7-point rule. Novel treatments disagreeing with peer-reviewed publications predominantly referred to “lumps,” with some cryptic forms united into single species because of the method's inability to accommodate molecular and massive bioacoustic datasets.
We also subjected 20 controversial cases to 7-point scoring by 26 ornithologists and observed a wide score variance, straddling from far below to above the 7-point species threshold and casting doubt on claims of high reproducibility.
We recommend against the adoption of the 7-point rule by taxonomic authorities, although it may continue to be a good informal approach to flag potential splits.
Studying macroevolutionary patterns of phenotypic variation and their driving forces in large radiations can shed light on how biodiversity is generated across broad spatiotemporal scales. In this study, we integrated song and morphological variation across more than 300 species representing the largest family of songbirds, the tanagers (Thraupidae), to uncover how morphological variables of the vocal tract combine to shape vocal evolution on a macroevolutionary scale. We found that body size correlated with multiple frequency parameters, concurring with past studies that show how body size constrains vocal evolution. Furthermore, bill size predicted multiple frequency and temporal song characters while bill shape was strongly associated with trill rates, suggesting that bill size and shape both constrain distinct elements of avian song independently of body size covariation. Our results demonstrate that the relationship between morphology and song exhibits modular variation when expanded to a macroevolutionary scale. Furthermore, our study emphasizes the need to consider multiple components of the avian vocal tract when exploring the macroevolutionary interplay of morphological traits and acoustic signals.
LAY SUMMARY
Avian vocalizations vary widely among birds and are associated with multiple aspects of their biology, including mechanisms of sexual selection, habitat acoustics, and avian vocal tract morphology.
The avian vocal tract is composed of many internal and external traits, but relatively few studies have disentangled the impact of multiple avian tract components on the evolution of bird song.
In this study, we quantify associations between 11 song variables and tarsus length (representing body size), bill size, and bill shape used in courtship displays of tanagers, the largest family of songbirds.
We find that both body size and bill morphology (size and shape) are correlated with various aspects of tanager song.
Taken together, different components of the avian vocal tract selectively constrain unique aspects of their vocalizations.
Future studies could examine internal (e.g., tracheal and syringeal) morphological traits in combination with bill morphology to gain a more comprehensive insight into how different elements of the avian vocal tract shape avian vocalizations.
SPECIAL FEATURE: SPECIES LIMITS AND TAXONOMY IN BIRDS
Four main challenges that can underpin ongoing, intransigent debates about species limits in birds are reviewed: allopatry (population subdivision vs. speciation), geographically widespread introgression of mitochondrial DNA (mtDNA), recent speciation, and selection. Examples from birds of the Australian region show how these challenges, their interplay, and the molecular-phenotypic discordance they generate can clarify or mislead species limits. Examples of how phylogenetic frameworks help reject or retain hypotheses of species limits under these challenges are given. Although mtDNA's strengths and limitations are well known, an underappreciated limitation of mtDNA is geographically widespread introgression that homogenizes mtDNA diversity across species, subspecies, or population boundaries and across hundreds of kilometers. The resulting discordance between mtDNA and phenotype can be profound. If undetected, the setting of species limits and evolutionarily significant units are misled. An example shows how recent genomic analyses can detect and solve the problem. Other examples concern legacy mtDNA-only datasets. These are often essentially unfinished studies leaving residual uncertainty in species limits. Examples illustrate when the possibility of large-scale introgression across species boundaries needs to be considered, and how genomic scale data offer solutions. Researchers must carefully parse 3 questions: has there been introgression of mtDNA and, if so, which population genetics-based driver has caused introgression, and do species limits need altering? Understanding of allopatry, mtDNA introgression, recent speciation, and selection must be properly integrated if species limits are to be robustly understood and applied with maximum benefit in downstream applications such as conservation and management.
LAY SUMMARY
Biologists still debate what species are and how we should best demarcate one species from another.
The debates reflect a curious aspect of ongoing evolution: although we expect each species to have its own unique DNA, that is often not the case for many pieces of DNA that we look at.
My paper reviews some of the major reasons why each species may not have its own unique DNA.
I focus on birds of the Australian region but the lessons apply to ornithologists everywhere.
This is important because we want to use DNA wisely to work out which populations and individuals belong to which species.
Then we can best conserve and manage the biodiversity that nurtures us in so many ways.
I hope my article will guide ornithologists everywhere in how they might deal with the thorny issues associated with these debates.
Prinias (Cisticolidae: Prinia) are resident warblers of open areas across Africa and Asia and include many polytypic species whose species limits have not been seriously reevaluated recently. Based on an integrative taxonomic analysis of morphology, song, and mitochondrial DNA (mtDNA), we suggest that 2 species should be recognized in the Graceful Prinia (Prinia gracilis) complex. In addition, our morphological analyses show the existence of a well-marked undescribed form in southeastern Somalia, which we name herein as a new subspecies. Prinia gracilis is a small, drab, long-tailed species with streaking above and plain pale underparts that has been suggested to fall into 2 groups: the southwestern nominate group (from Egypt to Oman) and the northeastern lepida group (from Turkey through India). However, the characters presented to justify this grouping are variable and show a mosaic pattern, and whether genetic and vocal differences exist is unknown. We found consistent between-group song differences, with the nominate group giving consistently longer inter-phrase intervals, whereas the members of the lepida group sing an essentially continuous reel. An mtDNA tree suggests a deep split between the nominate and lepida groups, with a coalescence time between these clades of ∼ 2.2 million years ago. Vocal and mtDNA analyses provided evidence that the northeastern Arabian Peninsula taxon carpenteri belongs to the lepida group. We found that, of all the morphological characters proposed, only proportions and tail barring and spotting relatively consistently distinguish the 2 groups. However, these characters strongly suggest that the eastern Arabian Peninsula is populated by taxa of both the gracilis and lepida groups, in different areas, but we lack genetic and bioacoustic data to corroborate this. Although further study is needed in potential contact zones, we suggest that 2 species should be recognized in the P. gracilis complex, and we propose the retention of the English name Graceful Prinia for P. gracilis sensu stricto, while we suggest that P. lepida be known as Delicate Prinia.
LAY SUMMARY
The Graceful Prinia is shown to be comprised of two groups differing in song, in mitochondrial DNA (mtDNA), and subtly in plumage and structure.
One group (the southwestern group) occurs from Egypt through Somalia and the Arabian Peninsula, while the other (the northeastern group) occurs from Turkey through northeastern India and Bangladesh.
Both groups vary extensively, but the southwestern group is slightly larger but shorter-tailed, with less distinct barring on the uppertail but more distinct dark spots on the undertail, than the northeastern group.
The southwestern group sings with clearly separated short phrases, whereas the northeastern group has a continuously reeling song.
MtDNA suggests that the two groups diverged ∼2.2 million years ago.
On the eastern Arabian Peninsula, populations of both groups evidently occur.
We suggest that these two groups should be recognized as separate species.
We evaluated the utility of new analyses of plumage and structure in this case and found that they add substantial value to integrative analyses determining species limits.
Species are fundamental to biology, conservation, and environmental legislation; yet, there is often disagreement on how and where species limits should be drawn. Even sophisticated molecular methods have limitations, particularly in the context of geographically isolated lineages or inadequate sampling of loci. With extinction rates rising, methods are needed to assess species limits rapidly but robustly. Tobias et al. devised a points-based system to compare phenotypic divergence between taxa against the level of divergence in sympatric species, establishing a threshold to guide taxonomic assessments at a global scale. The method has received a mixed reception. To evaluate its performance, we identified 397 novel taxonomic splits from 328 parent taxa made by application of the criteria (in 2014–2016) and searched for subsequent publications investigating the same taxa with molecular and/or phenotypic data. Only 71 (18%) novel splits from 60 parent taxa have since been investigated by independent studies, suggesting that publication of splits underpinned by the criteria in 2014–2016 accelerated taxonomic decisions by at least 33 years. In the evaluated cases, independent analyses explicitly or implicitly supported species status in 62 (87.3%) of 71 splits, with the level of support increasing to 97.2% when excluding subsequent studies limited only to molecular data, and reaching 100% when the points-based criteria were applied using recommended sample sizes. Despite the fact that the training set used to calibrate the criteria was heavily weighted toward passerines, splits of passerines and non-passerines received equally strong support from independent research. We conclude that the method provides a useful tool for quantifying phenotypic divergence and fast-tracking robust taxonomic decisions at a global scale.
LAY SUMMARY
A scoring system based on quantitative criteria was developed for classifying bird species and applied to the global avifauna in 2014–2016.
We assess the performance of the criteria by searching for independent taxonomic assessments published subsequently.
A minimum of 87% of novel taxonomic splits proposed by the criteria are supported by independent research, increasing to 97–100% when focusing only on integrative analyses based on genotypic and phenotypic information, or when the criteria were applied using more robust samples of individuals.
The proportion of novel splits assessed by subsequent independent studies suggests that the application of the criteria in 2014–2016 accelerated taxonomic decisions by at least 33 years.
We conclude that the criteria offer a useful tool for fast-tracking robust taxonomic decisions, although they do not remove the need for verification by more sophisticated analyses.
Despite the acknowledged importance of defining avian species limits to scientific research, conservation, and management, in practice, they often remain contentious. This is true even among practitioners of a single species concept and is inevitable owing to the continuous nature of the speciation process, our incomplete and changing understanding of individual cases, and differing interpretations of available data. This issue of Ornithology brings together several papers on species limits, some more theoretical and general, and others case studies of specific taxa. These are viewed primarily through the lens of the biological species concept (BSC), by far the most widely adopted species concept in influential ornithological works. The more conceptual contributions focus on the importance of the integrative approach in species delimitation; the importance of considering selection with the increasing use of genomic data; examinations of the effectiveness of the Tobias et al. character-scoring species limits criteria; a review of thorny issues in species delimitation using examples from Australo-Papuan birds; and a review of the process of speciation that addresses how population divergence poses challenges. Case studies include population genomics of the American Kestrel (Falco sparverius); an integrative taxonomic analysis of Graceful Prinia (Prinia gracilis) that suggests two species are involved; and a reevaluation of species limits in Caribbean Sharp-shinned Hawk (Accipiter striatus) taxa.
LAY SUMMARY
We provide a brief overview of the science of biodiversity and how it is applied to categorize organisms, particularly at the species level.
Speciation is a divergence process with an outcome that might produce species but often does not.
This process is continuous, but our taxonomic categories are discrete, so it can be difficult to determine exactly where a divergent population fits in our categorization scheme.
Ongoing changes in knowledge, sampling, data, and interpretation are leading to many improvements in the delimitation of bird species limits.
A series of articles in this issue of Ornithology make it clear that progress (and changes) will continue to be made, especially when using approaches that integrate information from multiple datasets.
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