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Species limits and taxonomy in birds

Species limits and taxonomy in birds Abstract 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. RESUMEN A pesar de la reconocida importancia de definir los límites de las especies de aves para la investigación científica, la conservación y el manejo, en la práctica a menudo siguen siendo polémicos. Esto es verdad incluso entre los que adhieren a un único concepto de especie, y es inevitable debido a la naturaleza continua del proceso de especiación, a nuestro entendimiento incompleto y cambiante de casos individuales, y a diferentes interpretaciones de los datos disponibles. Este número de Ornithology reúne varios artículos sobre los límites de las especies, algunos más teóricos y generales, y otros de casos de estudio de taxones específicos. Estos son vistos principalmente a través del lente del concepto biológico de especie (CBE), por lejos el concepto de especie más ampliamente adoptado en los trabajos ornitológicos influyentes. Las contribuciones más conceptuales se enfocan en la importancia del enfoque integrativo en la delimitación de las especies; la importancia de considerar la selección con el uso creciente de datos genómicos; el examen de la eficacia del criterio del límite de las especies de Tobias et al.; una revisión de cuestiones espinosas sobre la delimitación de especies utilizando ejemplos de aves de Australia y Nueva Guinea; y una revisión del proceso de especiación que aborda cómo la divergencia poblacional plantea desafíos. Los casos de estudio incluyen genómica poblacional de Falco sparverius; un análisis taxonómico integral de Prinia gracilis que sugiere que están involucradas dos especies; y una re-evaluación de los límites de las especies en los taxones de Accipiter striatus. 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. INTRODUCTION Species are among the most fundamental units of biology. It is important to describe and label them appropriately because species can receive more attention both in scientific studies and in conservation and management planning and funding than subspecies (e.g., McClure et al. 2020). Because of the appeal and ubiquity of birds and the popularity of birding, ornithology also has an immense public, for many of whom species limits are a major concern. The description of biodiversity (taxonomy and nomenclature) and the study of its relationships (phylogenetics and population comparisons) represent a mix of observational-comparative and hypothesis-testing approaches. These two groups of methodologies have been particularly powerful in the growth of biology (Mayr 1982), and remain so, for good reason: A solid descriptive and comparative basis enables the development of insightful hypotheses and experiments to better understand the processes and phenomena giving rise to the components and variations of life. Most specimens in museum collections, for example, stem from endeavors representing discovery, description, and comparison, and subsequently they form the basis for hypothesis testing among diverse research pursuits. Until we have an accurate, stable, and dependable taxonomy, we can expect this methodological combination to continue to yield a rich harvest in the science of avian diversity, particularly at the species level and below. Speciation is a divergence process between two or more groups of individuals that begins at shallow levels of divergence and proceeds toward species as a possible outcome. In the full process, with a reduction or cessation of gene flow between them, populations undergo a progression from undifferentiated to becoming so different that viable offspring can no longer be produced between individuals from the divergent groups. Different species concepts treat the threshold of speciation differently along this divergence trajectory. The biological species concept (BSC), the overwhelmingly dominant concept used in the world’s bird field guides and checklists, holds that “species are groups of interbreeding natural populations that are reproductively isolated from other such groups” (Mayr 1996). Despite the widespread use of the BSC, however, other species concepts include, most prominently, the phylogenetic species concept and the evolutionary species concept (Coyne and Orr 2004). Gill (2014) suggested that we adopt a new null hypothesis regarding biological species, one emphasizing distinct and reciprocally monophyletic taxa as indicative of reproductive isolation. One problem with this approach is that those criteria demonstrably fit many subspecies that are not reproductively isolated, and that levels of divergence matter. Another is that diagnosability as a central criterion risks an almost bottomless well of more and more finely divided “species,” dependent more on data and analytical tools than on factors that ultimately cause reproductive isolation. Toews (2015) considered the major ideological shift proposed by Gill (2014) to be unwarranted, and that taxonomic decisions should continue to be based on the best available evidence for reproductive isolation. Under the BSC, our null hypothesis is probably best phrased thus: “Allopatric populations of birds that are similar would probably not show essential reproductive isolation if they were to occur in sympatry.” “Similar” here has historically meant levels of phenotypic divergence that are not equivalent to or above those exhibited by close relatives that do show essential reproductive isolation on contact. TAXONOMY Species delimitation involves the practical application of a species concept. But the application of taxonomy requires dividing the products of the gradual divergence process into sharply defined nomenclatural bins (e.g., subspecies, species) that often lack obvious traits delimiting the edges of those bins. This has been a problem in biology since its inception as a science (e.g., see Darwin [1859] on “Doubtful species”). In scientific nomenclature, we have subspecies and species to denote key stages of differentiation in this process. In practice, we often use additional labels along this divergence progression that provide more flexibility to denote levels of differentiation than formal taxonomic nomenclature provides (e.g., populations, management units, clines, evolutionarily significant units, [subspecies], subspecies groups, semispecies, [species], and species and superspecies complexes). The research approaches that we use to understand this diversity have important impacts on how we interpret results taxonomically. Phylogenetics, the study of relationships among life forms, uses a toolbox of theory and methodology that tends to break down at the shallow evolutionary levels at which the speciation process is occurring. This breakdown occurs because lineage history alone does not capture (and can be confounded by) other factors important in generating biodiversity (e.g., subspecies, species), such as selection, drift, gene flow, and fluctuating effective population sizes, each of which vary among lineages and can change through time (see also Rieppel 2010). An example of this breakdown is a species that comprises multiple lineages (e.g., with a series of island populations with low dispersal among islands following their colonization but before divergence proceeds so far that effective reproductive isolating mechanisms are present). A species can also found a different species lineage from within a complex of related lineages, producing a lack of monophyly for the originating (and still extant) species; for example, when an island is colonized from dispersal of a continental species and then through isolation and selection diverges to full speciation, while the continental populations continue on their own paths of relative isolation and gene flow. For the speciation process, historical relatedness at these levels (i.e., in the purview of systematics and phylogeography) matters less than ongoing connectivity, gene flow, selection, and drift. At these shallow, more recent levels, populational processes dominate (e.g., gene trees vs species trees), and the theories and toolboxes of population-level studies (e.g., in genomics and phenomics) come more strongly into play. As Avise and Wollenberg (1997) pointed out, understanding speciation is best accomplished through integration of these macro- and micro-evolutionary perspectives. Among ornithologists, we find widespread concern that there are many taxa that are overlumped (e.g., multiple good species are wrongly considered to be just one), but also many taxa that are oversplit (e.g., too many subspecies have wrongly been raised to full species status). There are probably fewer cases of oversplitting than overlumping at present. In part, this issue is conceptual (i.e., disagreements on species concepts), but even among the major checklists that adopt the BSC, there are many disagreements at the species level. This indicates that there is a lot of research and taxonomic work remaining to be done to get to a thorough and even treatment of species-level taxa among birds (and we have yet to really try to make our species-level taxa equivalent to those in other groups, e.g., plants, insects). One overarching theme in recent taxonomic research is the need for it to be integrative, that is to include multiple lines of evidence that are useful when inferring reproductive isolation to determine species limits. While this has been an important component of taxonomy for decades (Mayr et al. 1953, Simpson 1961, Mayr 1969, Mayr and Ashlock 1991), repeated efforts to simplify analyses to provide definitive answers have produced successive waves of hopeful pursuits that have not proven universally useful or acceptable, and some of these continue to play out today. Examples include phenetics and numerical taxonomy, mitochondrial DNA (mtDNA) monophyly or barcode gaps, character scoring methods (Tobias et al. 2010), and genomic clustering methods (e.g., Yang and Rannala 2010). This is not to say that these methodological approaches lack scientific merit (see, e.g., how key aspects of numerical taxonomy have remained useful; Sneath 1995). But despite their appeal, they have been either largely abandoned or not widely taken up as general approaches to delimit biological species of birds (at least) because of demonstrable limitations, including outright errors (e.g., Mayr 1965, Funk and Omland 2003, Sukumaran and Knowles 2017, Rheindt and Ng 2021). Finally, diagnosability alone has not been widely adopted for species delimitation because it is easily achieved evolutionarily, especially genetically, and so it is common among shallowly diverged populations. SPECIES LIMITS In this issue of Ornithology, a series of articles addresses some of the major challenges in species delimitation and demonstrates and discusses ways in which researchers are making progress on elucidating avian divergence and applying taxonomy at species and subspecies levels. These articles comprise both reviews and applications. A common theme among them is the need for integrative research; concordance among multiple datasets improves delimitation of species and subspecies. Cicero et al. (2021) considered integrative taxonomy itself and its most important aspects in birds. They also examined the practical aspects of determining avian species limits using this approach. They included data and analyses from recent taxonomic decisions of the North American Classification Committee of the American Ornithological Society and provided a summary and recommendations for studies that have species limits implications. Cadena and Zapata (2021) addressed the increasing use of genomic data in species delimitation and some of the main problems in doing so, including an exclusive focus on genomics and gene flow. They reviewed examples showing how critical it is to consider selection—through phenotypic data and analyses—to improve our abilities to define evolutionary lineages. Rheindt and Ng (2021) examined the Tobias et al.(2010) criteria for determining species limits by empirically testing these criteria for reproducibility in character scoring. Their results raise doubts about the reproducibility of this method among ornithologists and indicate that it might be too conservative, as in their tests it missed cryptic species in the Indonesian Archipelago. They suggested that this methodology can serve as an exploratory tool but that it should not be more widely adopted as a standalone approach. Tobias et al. (2021) also examined the Tobias et al.(2010) criteria, but they did so in terms of how applications of the method from 2014 to 2016 had fared under independent examination. Of 71 taxonomic splits they had made using these criteria that were subsequently studied by others using other methodologies, >87% have been supported. They suggested that the method is useful both for rapid, generally robust taxonomic decision-making and for evaluating changes that are proposed using other methods. Joseph (2021) considered Australo-Papuan avian examples to illustrate four main challenges that produce ongoing debates about species limits: allopatry, introgression of mtDNA, recent speciation, and selection. Many of these example cases remain to be fully resolved, and Joseph (2021) provided a series of additional examples that give future researchers rich ground to work. Winker (2021) reviewed the process of speciation and addressed aspects of population divergence and associated data that often make it challenging to determine species limits. He addressed areas such as single-locus criteria, gene flow, the comparative method, stochastic processes vs selection, speciation stalled just short of completion, and assortative mating. Each has proven problematic in determining species limits and requires clear-eyed evaluation. Ruegg et al. (2021) used population genomics to examine intraspecific divergences from population to subspecies levels in the American Kestrel (Falco sparverius) across the United States and Canada. Their work provides a genomic view of diversity within this species, partly in relation to described subspecific diversity but going beyond that to consider other population attributes. Their genoscape (the mapping of genetic variation across a species’ range) provides support not only for the two subspecies currently recognized in this part of the species’ range, but also for five populations that correspond to migration phenotypes. While we should not expect correlations between genomic markers and subspecific characters, this study provides a good example of how genomic data can help us understand population divergence in phenotypic and genotypic terms, informing both evolutionary biology and management. Alström et al. (2021) used integrative taxonomic analyses to show that the Graceful Prinia (Prinia gracilis) complex comprises two cryptic lineages that may be best considered species. They showed for the first time that the two major subspecific groups have diverged substantially in song and mtDNA, and that analyses of the more limited morphological differences nevertheless seem informative with respect to species delimitation. Catanach et al. (2021) addressed the issue of species limits within Caribbean Sharp-shinned Hawks (Accipiter striatus) using ultraconserved elements (UCEs), mtDNA, and single-nucleotide polymorphisms (SNPs). Based on these datasets, they suggested that lack of gene flow has led to divergence consistent with species-level treatment in the endangered taxa of Puerto Rico (venator), Hispaniola (striatus), and Cuba (fringilloides). LOOKING FORWARD These are exciting times for speciation research and for improving our taxonomy by more accurately determining species limits. Researchers whose work bears on species limits would best serve their readers by stating how their findings fit or do not fit current taxonomic hypotheses and suggesting appropriate change(s) when their data support modifying current hypotheses. If their research leaves some questions open, they might help future workers by pointing out where further data could be informative. It will also be helpful to interpret results under different species concepts when substantial numbers of taxonomists advocate for one concept over another. In this world of greater collaboration, reproducibility, and dispersed but aggregable data, best practices need to be followed in specimen and data preservation and archiving, in accessibility, and in proper specimen citation. This includes use of publicly open and online data and specimen repositories. It is clear that the study of avian divergence and the testing of taxonomic hypotheses will continue to develop and employ big data (e.g., in genomics, phenomics, environmental data, etc.). We anticipate that, as in the past, evolutionary biologists and taxonomists will accommodate and welcome this new information that will help us understand the endlessly fascinating diversity of birds. ACKNOWLEDGMENTS We thank the authors and the presenters who contributed to this series of articles and to the “Species Limits in Birds: Integrative and Practical Considerations for Taxonomy” symposium that we held at the 2019 American Ornithological Society meeting in Anchorage, Alaska. We also thank an anonymous reviewer for comments on an earlier draft. Author contributions: Both authors conceived, outlined, and wrote the paper. Conflict of interest statement: The authors declare that they have no conflicts. LITERATURE CITED Alström, P., P. C. Rasmussen, C. Xia, L. Zhang, C. Liu, J. Magnusson, A. Shafaeipour,and U. Olsson (2021). Morphology, vocalizations, and mitochondrial DNA suggest that the Graceful Prinia is two species. Ornithology 138: 1 – 23 . doi:10.1093/ornithology/ukab014 Google Scholar OpenURL Placeholder Text WorldCat Avise , J. C. , and K. Wollenberg ( 1997 ). Phylogenetics and the origin of species . Proceedings of the National Academy of Sciences USA 94 : 7748 – 7755 . Google Scholar Crossref Search ADS WorldCat Cadena , C. D. , and F. Zapata ( 2021 ). The genomic revolution and species delimitation in birds (and other organisms): Why phenotypes should not be overlooked . Ornithology 138 : 1 – 18 . doi:10.1093/ornithology/ukaa069 Google Scholar OpenURL Placeholder Text WorldCat Catanach , T. A. , M. R. Halley, J. M. Allen, J. A. Johnson, R. Thorstrom, S. Palhano, C. P. Thunder, J. C. Gallardo, and J. D. Weckstein ( 2021 ). Systematics and conservation of an endemic radiation of Accipiter hawks in the Caribbean islands . Ornithology 138 . In press . Google Scholar OpenURL Placeholder Text WorldCat Cicero , C. , N. A. Mason, R. A. Jiménez , D. R. Wait, C. Y. Wang-Claypool, and R. C. K. Bowie ( 2021 ). Integrative taxonomy and geographic sampling underlie successful species delimitation . Ornithology 138 : 1 – 15 . doi:10.1093/ornithology/ukab009 Google Scholar OpenURL Placeholder Text WorldCat Coyne , J. A. , and H. A. Orr ( 2004 ). Speciation . Sinauer Associates , Sunderland, MA, USA . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Darwin , C . ( 1859 ). On the Origin of Species . John Murray , London, UK . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Funk , D. J. , and K. E. Omland ( 2003 ). Species-level paraphyly and polyphyly: Frequency, causes, and consequences, with insights from animal mitochondrial DNA . Annual Review of Ecology, Evolution, and Systematics 34 : 397 – 423 . Google Scholar Crossref Search ADS WorldCat Gill , F. B . ( 2014 ). Species taxonomy of birds: Which null hypothesis? The Auk 131 : 150 – 161 . Google Scholar Crossref Search ADS WorldCat Joseph , L . ( 2021 ). Species limits in birds: Australian perspectives on inter-related challenges of allopatry, introgression of mitochondrial DNA, recent speciation, and selection . Ornithology 138 : 1 – 15 . doi:10.1093/ornithology/ukab012 Google Scholar OpenURL Placeholder Text WorldCat Mayr , E . ( 1965 ). Numerical phenetics and taxonomic theory . Systematic Zoology 14 : 73 – 97 . Google Scholar Crossref Search ADS WorldCat Mayr , E . ( 1969 ). Principles of Systematic Zoology . McGraw-Hill , New York, NY, USA . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Mayr , E . ( 1982 ). The Growth of Biological Thought . Belknap Press , Cambridge, MA, USA . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Mayr , E . ( 1996 ). What is a species, and what is not? Philosophy of Science 63 : 262 – 277 . Google Scholar Crossref Search ADS WorldCat Mayr , E. , and P. D. Ashlock ( 1991 ). Principles of Systematic Zoology , 2nd ed. McGraw-Hill, New York, NY, USA . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Mayr , E. , E. G. Linsley, and R. L. Usinger ( 1953 ). Methods and Principles of Systematic Zoology . McGraw-Hill , New York, NY, USA . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC McClure , C. J. W. , D. Lepage, L. Dunn, D. L. Anderson, S. E. Schulwitz, L. Camacho, B. W. Robinson, L. Christidis, T. S. Schulenberg, M. J. Iliff, et al. ( 2020 ). Towards reconciliation of the four world bird lists: Hotspots of disagreement in taxonomy of raptors . Proceedings of the Royal Society B: Biological Sciences 287 : 20200683 . Google Scholar Crossref Search ADS WorldCat Rheindt , F. , and E. Y. X. Ng ( 2021 ). Avian taxonomy in turmoil: The 7-point rule is poorly reproducible and may overlook substantial cryptic diversity . Ornithology 138 : 1 – 11 . doi:10.1093/ornithology/ukab010 Google Scholar OpenURL Placeholder Text WorldCat Rieppel , O . ( 2010 ). Species monophyly . Journal of Zoological Systematics and Evolutionary Research 48 : 1 – 8 . Google Scholar Crossref Search ADS WorldCat Ruegg , K. C. , M. Brinkmeyer, C. M. Bossu, R. A. Bay, E. C. Anderson, C. W. Boal, R. D. Dawson, A. Eschenbauch, C. J. W. McClure, K. E. Miller, et al. ( 2021 ). The American Kestrel (Falco sparverius) genoscape: Implications for monitoring, management, and subspecies boundaries . Ornithology 138 : 000 – 000 . Google Scholar OpenURL Placeholder Text WorldCat Simpson , G. G . ( 1961 ). Principles of Animal Taxonomy . Columbia University Press , New York, NY, USA . Google Scholar Crossref Search ADS Google Preview WorldCat COPAC Sneath , P. H. A . ( 1995 ). Thirty years of numerical taxonomy . Systematic Biology 44 : 281 – 298 . Google Scholar Crossref Search ADS WorldCat Sukumaran , J. , and L. L. Knowles ( 2017 ). Multispecies coalescent delimits structure, not species . Proceedings of the National Academy of Sciences USA 114 : 1607 – 1612 . Google Scholar Crossref Search ADS WorldCat Tobias, J. A., N. Seddon, C. N. Spottiswoode, J. D. Pilgrim, L. D. C. Fishpool, and N. J. Collar (2010). Quantitative criteria for species delimitation. Ibis 152: 724 – 746 . Google Scholar Crossref Search ADS WorldCat Tobias , J. A. , P. F. Donald, R. W. Martin, S. H. M. Butchart, and N. J. Collar ( 2021 ). Performance of a points-based scoring system for assessing species limits in birds . Ornithology 138 : 1 – 14 . doi:10.1093/ornithology/ukab016 Google Scholar OpenURL Placeholder Text WorldCat Toews , D. P. L . ( 2015 ). Biological species and taxonomic species: Will a new hypothesis help? (A comment on Gill 2014) . The Auk: Ornithological Advances 132 : 78 – 81 . Google Scholar Crossref Search ADS WorldCat Winker , K . ( 2021 ). An overview of speciation and species limits in birds . Ornithology 138 : 1 – 27 . doi:10.1093/ornithology/ukab006 Google Scholar OpenURL Placeholder Text WorldCat Yang , Z. , and B. Rannala ( 2010 ). Bayesian species delimitation using multilocus sequence data . Proceedings of the National Academy of Sciences USA 107 : 9264 – 9269 . Google Scholar Crossref Search ADS WorldCat Copyright © American Ornithological Society 2021. All rights reserved. For permissions, e-mail: journals.permissions@oup.com. 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Species limits and taxonomy in birds

Winker, Kevin; Rasmussen, Pamela C
Ornithology , Volume Advance Article – Apr 8, 2021
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Abstract

Abstract 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. RESUMEN A pesar de la reconocida importancia de definir los límites de las especies de aves para la investigación científica, la conservación y el manejo, en la práctica a menudo siguen siendo polémicos. Esto es verdad incluso entre los que adhieren a un único concepto de especie, y es inevitable debido a la naturaleza continua del proceso de especiación, a nuestro entendimiento incompleto y cambiante de casos individuales, y a diferentes interpretaciones de los datos disponibles. Este número de Ornithology reúne varios artículos sobre los límites de las especies, algunos más teóricos y generales, y otros de casos de estudio de taxones específicos. Estos son vistos principalmente a través del lente del concepto biológico de especie (CBE), por lejos el concepto de especie más ampliamente adoptado en los trabajos ornitológicos influyentes. Las contribuciones más conceptuales se enfocan en la importancia del enfoque integrativo en la delimitación de las especies; la importancia de considerar la selección con el uso creciente de datos genómicos; el examen de la eficacia del criterio del límite de las especies de Tobias et al.; una revisión de cuestiones espinosas sobre la delimitación de especies utilizando ejemplos de aves de Australia y Nueva Guinea; y una revisión del proceso de especiación que aborda cómo la divergencia poblacional plantea desafíos. Los casos de estudio incluyen genómica poblacional de Falco sparverius; un análisis taxonómico integral de Prinia gracilis que sugiere que están involucradas dos especies; y una re-evaluación de los límites de las especies en los taxones de Accipiter striatus. 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. INTRODUCTION Species are among the most fundamental units of biology. It is important to describe and label them appropriately because species can receive more attention both in scientific studies and in conservation and management planning and funding than subspecies (e.g., McClure et al. 2020). Because of the appeal and ubiquity of birds and the popularity of birding, ornithology also has an immense public, for many of whom species limits are a major concern. The description of biodiversity (taxonomy and nomenclature) and the study of its relationships (phylogenetics and population comparisons) represent a mix of observational-comparative and hypothesis-testing approaches. These two groups of methodologies have been particularly powerful in the growth of biology (Mayr 1982), and remain so, for good reason: A solid descriptive and comparative basis enables the development of insightful hypotheses and experiments to better understand the processes and phenomena giving rise to the components and variations of life. Most specimens in museum collections, for example, stem from endeavors representing discovery, description, and comparison, and subsequently they form the basis for hypothesis testing among diverse research pursuits. Until we have an accurate, stable, and dependable taxonomy, we can expect this methodological combination to continue to yield a rich harvest in the science of avian diversity, particularly at the species level and below. Speciation is a divergence process between two or more groups of individuals that begins at shallow levels of divergence and proceeds toward species as a possible outcome. In the full process, with a reduction or cessation of gene flow between them, populations undergo a progression from undifferentiated to becoming so different that viable offspring can no longer be produced between individuals from the divergent groups. Different species concepts treat the threshold of speciation differently along this divergence trajectory. The biological species concept (BSC), the overwhelmingly dominant concept used in the world’s bird field guides and checklists, holds that “species are groups of interbreeding natural populations that are reproductively isolated from other such groups” (Mayr 1996). Despite the widespread use of the BSC, however, other species concepts include, most prominently, the phylogenetic species concept and the evolutionary species concept (Coyne and Orr 2004). Gill (2014) suggested that we adopt a new null hypothesis regarding biological species, one emphasizing distinct and reciprocally monophyletic taxa as indicative of reproductive isolation. One problem with this approach is that those criteria demonstrably fit many subspecies that are not reproductively isolated, and that levels of divergence matter. Another is that diagnosability as a central criterion risks an almost bottomless well of more and more finely divided “species,” dependent more on data and analytical tools than on factors that ultimately cause reproductive isolation. Toews (2015) considered the major ideological shift proposed by Gill (2014) to be unwarranted, and that taxonomic decisions should continue to be based on the best available evidence for reproductive isolation. Under the BSC, our null hypothesis is probably best phrased thus: “Allopatric populations of birds that are similar would probably not show essential reproductive isolation if they were to occur in sympatry.” “Similar” here has historically meant levels of phenotypic divergence that are not equivalent to or above those exhibited by close relatives that do show essential reproductive isolation on contact. TAXONOMY Species delimitation involves the practical application of a species concept. But the application of taxonomy requires dividing the products of the gradual divergence process into sharply defined nomenclatural bins (e.g., subspecies, species) that often lack obvious traits delimiting the edges of those bins. This has been a problem in biology since its inception as a science (e.g., see Darwin [1859] on “Doubtful species”). In scientific nomenclature, we have subspecies and species to denote key stages of differentiation in this process. In practice, we often use additional labels along this divergence progression that provide more flexibility to denote levels of differentiation than formal taxonomic nomenclature provides (e.g., populations, management units, clines, evolutionarily significant units, [subspecies], subspecies groups, semispecies, [species], and species and superspecies complexes). The research approaches that we use to understand this diversity have important impacts on how we interpret results taxonomically. Phylogenetics, the study of relationships among life forms, uses a toolbox of theory and methodology that tends to break down at the shallow evolutionary levels at which the speciation process is occurring. This breakdown occurs because lineage history alone does not capture (and can be confounded by) other factors important in generating biodiversity (e.g., subspecies, species), such as selection, drift, gene flow, and fluctuating effective population sizes, each of which vary among lineages and can change through time (see also Rieppel 2010). An example of this breakdown is a species that comprises multiple lineages (e.g., with a series of island populations with low dispersal among islands following their colonization but before divergence proceeds so far that effective reproductive isolating mechanisms are present). A species can also found a different species lineage from within a complex of related lineages, producing a lack of monophyly for the originating (and still extant) species; for example, when an island is colonized from dispersal of a continental species and then through isolation and selection diverges to full speciation, while the continental populations continue on their own paths of relative isolation and gene flow. For the speciation process, historical relatedness at these levels (i.e., in the purview of systematics and phylogeography) matters less than ongoing connectivity, gene flow, selection, and drift. At these shallow, more recent levels, populational processes dominate (e.g., gene trees vs species trees), and the theories and toolboxes of population-level studies (e.g., in genomics and phenomics) come more strongly into play. As Avise and Wollenberg (1997) pointed out, understanding speciation is best accomplished through integration of these macro- and micro-evolutionary perspectives. Among ornithologists, we find widespread concern that there are many taxa that are overlumped (e.g., multiple good species are wrongly considered to be just one), but also many taxa that are oversplit (e.g., too many subspecies have wrongly been raised to full species status). There are probably fewer cases of oversplitting than overlumping at present. In part, this issue is conceptual (i.e., disagreements on species concepts), but even among the major checklists that adopt the BSC, there are many disagreements at the species level. This indicates that there is a lot of research and taxonomic work remaining to be done to get to a thorough and even treatment of species-level taxa among birds (and we have yet to really try to make our species-level taxa equivalent to those in other groups, e.g., plants, insects). One overarching theme in recent taxonomic research is the need for it to be integrative, that is to include multiple lines of evidence that are useful when inferring reproductive isolation to determine species limits. While this has been an important component of taxonomy for decades (Mayr et al. 1953, Simpson 1961, Mayr 1969, Mayr and Ashlock 1991), repeated efforts to simplify analyses to provide definitive answers have produced successive waves of hopeful pursuits that have not proven universally useful or acceptable, and some of these continue to play out today. Examples include phenetics and numerical taxonomy, mitochondrial DNA (mtDNA) monophyly or barcode gaps, character scoring methods (Tobias et al. 2010), and genomic clustering methods (e.g., Yang and Rannala 2010). This is not to say that these methodological approaches lack scientific merit (see, e.g., how key aspects of numerical taxonomy have remained useful; Sneath 1995). But despite their appeal, they have been either largely abandoned or not widely taken up as general approaches to delimit biological species of birds (at least) because of demonstrable limitations, including outright errors (e.g., Mayr 1965, Funk and Omland 2003, Sukumaran and Knowles 2017, Rheindt and Ng 2021). Finally, diagnosability alone has not been widely adopted for species delimitation because it is easily achieved evolutionarily, especially genetically, and so it is common among shallowly diverged populations. SPECIES LIMITS In this issue of Ornithology, a series of articles addresses some of the major challenges in species delimitation and demonstrates and discusses ways in which researchers are making progress on elucidating avian divergence and applying taxonomy at species and subspecies levels. These articles comprise both reviews and applications. A common theme among them is the need for integrative research; concordance among multiple datasets improves delimitation of species and subspecies. Cicero et al. (2021) considered integrative taxonomy itself and its most important aspects in birds. They also examined the practical aspects of determining avian species limits using this approach. They included data and analyses from recent taxonomic decisions of the North American Classification Committee of the American Ornithological Society and provided a summary and recommendations for studies that have species limits implications. Cadena and Zapata (2021) addressed the increasing use of genomic data in species delimitation and some of the main problems in doing so, including an exclusive focus on genomics and gene flow. They reviewed examples showing how critical it is to consider selection—through phenotypic data and analyses—to improve our abilities to define evolutionary lineages. Rheindt and Ng (2021) examined the Tobias et al.(2010) criteria for determining species limits by empirically testing these criteria for reproducibility in character scoring. Their results raise doubts about the reproducibility of this method among ornithologists and indicate that it might be too conservative, as in their tests it missed cryptic species in the Indonesian Archipelago. They suggested that this methodology can serve as an exploratory tool but that it should not be more widely adopted as a standalone approach. Tobias et al. (2021) also examined the Tobias et al.(2010) criteria, but they did so in terms of how applications of the method from 2014 to 2016 had fared under independent examination. Of 71 taxonomic splits they had made using these criteria that were subsequently studied by others using other methodologies, >87% have been supported. They suggested that the method is useful both for rapid, generally robust taxonomic decision-making and for evaluating changes that are proposed using other methods. Joseph (2021) considered Australo-Papuan avian examples to illustrate four main challenges that produce ongoing debates about species limits: allopatry, introgression of mtDNA, recent speciation, and selection. Many of these example cases remain to be fully resolved, and Joseph (2021) provided a series of additional examples that give future researchers rich ground to work. Winker (2021) reviewed the process of speciation and addressed aspects of population divergence and associated data that often make it challenging to determine species limits. He addressed areas such as single-locus criteria, gene flow, the comparative method, stochastic processes vs selection, speciation stalled just short of completion, and assortative mating. Each has proven problematic in determining species limits and requires clear-eyed evaluation. Ruegg et al. (2021) used population genomics to examine intraspecific divergences from population to subspecies levels in the American Kestrel (Falco sparverius) across the United States and Canada. Their work provides a genomic view of diversity within this species, partly in relation to described subspecific diversity but going beyond that to consider other population attributes. Their genoscape (the mapping of genetic variation across a species’ range) provides support not only for the two subspecies currently recognized in this part of the species’ range, but also for five populations that correspond to migration phenotypes. While we should not expect correlations between genomic markers and subspecific characters, this study provides a good example of how genomic data can help us understand population divergence in phenotypic and genotypic terms, informing both evolutionary biology and management. Alström et al. (2021) used integrative taxonomic analyses to show that the Graceful Prinia (Prinia gracilis) complex comprises two cryptic lineages that may be best considered species. They showed for the first time that the two major subspecific groups have diverged substantially in song and mtDNA, and that analyses of the more limited morphological differences nevertheless seem informative with respect to species delimitation. Catanach et al. (2021) addressed the issue of species limits within Caribbean Sharp-shinned Hawks (Accipiter striatus) using ultraconserved elements (UCEs), mtDNA, and single-nucleotide polymorphisms (SNPs). Based on these datasets, they suggested that lack of gene flow has led to divergence consistent with species-level treatment in the endangered taxa of Puerto Rico (venator), Hispaniola (striatus), and Cuba (fringilloides). LOOKING FORWARD These are exciting times for speciation research and for improving our taxonomy by more accurately determining species limits. Researchers whose work bears on species limits would best serve their readers by stating how their findings fit or do not fit current taxonomic hypotheses and suggesting appropriate change(s) when their data support modifying current hypotheses. If their research leaves some questions open, they might help future workers by pointing out where further data could be informative. It will also be helpful to interpret results under different species concepts when substantial numbers of taxonomists advocate for one concept over another. In this world of greater collaboration, reproducibility, and dispersed but aggregable data, best practices need to be followed in specimen and data preservation and archiving, in accessibility, and in proper specimen citation. This includes use of publicly open and online data and specimen repositories. It is clear that the study of avian divergence and the testing of taxonomic hypotheses will continue to develop and employ big data (e.g., in genomics, phenomics, environmental data, etc.). We anticipate that, as in the past, evolutionary biologists and taxonomists will accommodate and welcome this new information that will help us understand the endlessly fascinating diversity of birds. ACKNOWLEDGMENTS We thank the authors and the presenters who contributed to this series of articles and to the “Species Limits in Birds: Integrative and Practical Considerations for Taxonomy” symposium that we held at the 2019 American Ornithological Society meeting in Anchorage, Alaska. 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Published: Apr 8, 2021

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