Ornithology Program (HRC) Harry Reid Center for Environmental Studies

5-2001

The taxonomic rank of Spizella taverneri: A response to Mayr and Johnson

John Klicka University of Nevada, Las Vegas, [email protected]

Robert M. Zink University of Minnesota

Jon C. Barlow Royal Ontario Museum

W. Bruce McGillivray Provincial Museum of Alberta

Terry J. Doyle Ten Thousand Islands National Wildlife Refuge

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Repository Citation Klicka, J., Zink, R. M., Barlow, J. C., McGillivray, W. B., Doyle, T. J. (2001). The taxonomic rank of Spizella taverneri: A response to Mayr and Johnson. Condor, 103(2), 420-422. Available at: https://digitalscholarship.unlv.edu/hrc_ornithology/32

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The Condor 103:420±422 ᭧ The Cooper Ornithological Society 2001 lidad de la reproduccioÂn, vocalizaciones y morfologõÂa apoyaban el reconocimiento de S. taverneri como una especie tanto ®logeneÂtica como bioloÂgica. Nada en el comentario de Mayr y Johnson causa que cambiemos THE TAXONOMIC RANK OF SPIZELLA esa conclusioÂn. Creemos que es probable que ese par TAVERNERI: A RESPONSE TO MAYR AND de taxones alopaÂtricos esteÂn aislados. Contrariamente 1 a Mayr y Johnson, creemos que se proporciona maÂs JOHNSON informacioÂn designando a S. taverneri como especie, pues revela el hecho de que ambos son taxones que JOHN KLICKA,2 Marjorie Barrick Museum of Natural evolucionan independientemente. La clasi®cacioÂn de History, Box 454012, University of Nevada Las Ve- Spizella debe mostrar el estatus de especies hermanas gas, 4505 Maryland Parkway, Las Vegas, NV 98154- de S. taverneri y S. breweri, sin tomar en cuenta para 4012 el balance el grado de divergencia de las secuencias entre las especies, como fue sugerido por Mayr y John- ROBERT M. ZINK, J. F. Bell Museum of Natural His- tory, 100 Ecology Building, University of Minnesota, son. St. Paul, MN 55108 Mayr and Johnson (2001) do not dispute the evidence JON C. BARLOW, Royal Ontario Museum, 100 Queen's presented by Klicka et al. (1999) that corroborated the Park, Toronto, ON M5S 2C6, Canada existence of a taxon named taverneri. The discussion W. B RUCE MCGILLIVRAY, Provincial Museum of Alber- instead concerns whether this taxon should be ranked ta, 12856-102 Avenue, Edmonton, AB T5N 0M6, Can- as a species or a subspecies. Mayr and Johnson believe ada that our evidence is best interpreted to indicate that taverneri is a subspecies of the biological species S. TERRY J. DOYLE, Ten Thousand Islands National Wild- breweri. We concluded that taverneri represents a life Refuge, 3860 Tollgate Blvd., Suite 300, Naples, FL newly evolved phylogenetic species, and probably a 34114 biological species as well. We believe that the argu- ments presented by Mayr and Johnson, grounded in Abstract. Mayr and Johnson suggest that Spizella the school of evolutionary systematics (Mayr and Ash- taverneri should be a subspecies of the biological lock 1991), are equivocal, and show why the biologi- species S. breweri, because it is possibly not repro- cal species concept (BSC) has been losing favor in ductively isolated. We originally concluded that evi- many disciplines (Wheeler and Meier 2000), including dence from mitochondrial DNA sequences, habitat preferences, timing of breeding, vocalizations, and ornithology (Zink and Davis 1999). Below we respond morphology supported the recognition of S. taverneri to the issues raised by Mayr and Johnson. as a phylogenetic and biological species. Nothing in Evidence for reproductive isolation. Mayr and John- the commentary by Mayr and Johnson causes us to son state that if genetic independence cannot be deter- change that conclusion. We believe that it is probable mined by direct observation (i.e., a ``test of sympat- that these two allopatric taxa are isolated. Contrary ry''), it must be inferred. This, in fact, has long been to Mayr and Johnson, we believe that more infor- recognized as a critical ¯aw in the biological species mation is given by ranking S. taverneri as a species, concept: the main criterion for ranking taxa as species because it reveals the fact that they are independently must be inferred in the thousands of cases (such as the evolving taxa. The classi®cation of Spizella should present one) in which diagnosable populations or convey the sister-species status of S. taverneri and S. groups of populations are allopatric. The methods of breweri, without regard for balancing the degree of inference are vague and vary among taxonomists. To- sequence divergence among species, as suggested by day, analyses of DNA are used to discover genetically Mayr and Johnson. isolated groups of populations and to recover their phylogenetic relationships. In modern systematics, the Key words: Brewer's Sparrow, classi®cation, DNA phylogeny is used for classi®cation (GutieÂrrez et al. sequences, species concepts, Timberline Sparrow. 2000), including the assignment of species limits (Zink and Davis 1999). Furthermore, it is now known that El Estatus TaxonoÂmico de Spizella the pattern of reproductive compatibility is not neces- taverneri: una Respuesta a Mayr y sarily an accurate predictor of phylogenetic relation- Johnson ship because non-sister taxa often hybridize (Zink and McKitrick 1995, Klicka et al. in press). Thus, species Resumen: Mayr y Johnson sugieren que Spizella limits based on recovered patterns of evolutionary his- taverneri debe ser una subespecie de la especie bio- tory (e.g., phylogenetic analyses of DNA) can con¯ict loÂgica S. breweri, porque posiblemente no se encuentra with those based on patterns of reproductive compat- aislada reproductivamente. Nosotros originalmente ibility. Zink and Davis (1999) suggested that the ap- concluimos que la evidencia de las secuencias del propriate research program was to map patterns of re- ADN mitocondrial, preferencias de haÂbitat, tempora- productive compatibility and isolation onto a phylog- eny. In this way, one can understand which character- istics contribute to reproductive compatibility and 1 Received 10 January 2001. Accepted 12 January isolation among taxa, rather than to use these catego- 2001. ries as ambiguous characters to diagnose species. 2 E-mail: [email protected] Our DNA analyses suggested that S. breweri and S. COMMENTARY 421 taverneri are recently isolated sister taxa. Whether they taken by Mayr and Johnson would have more validity are reproductively isolated is of interest, but is only if all subspecies were as clearly de®ned as S. taverneri relevant to determining whether S. taverneri is a bio- (although this would still not be an argument in favor logical species. Mayr and Johnson speculate that there of keeping the BSC, Zink and Davis 1999). Unfortu- is insuf®cient evidence to predict whether pairings be- nately, all subspecies are not created equal. The liter- tween individual S. taverneri and S. breweri would ature is fraught with poorly de®ned and indistinguish- yield viable offspring, were they to encounter each able subspecies. A growing body of evidence indicates other during the breeding season. We think that some that as many as 50% of avian subspecies are not cor- of the differences that help diagnose S. taverneri are roborated by mtDNA data, presumably because they relevant to the question of reproductive compatibility. are based on arbitrary divisions of single morpholog- For example, Mayr and Johnson disregard substantial ical character clines (Zink et al. 2000). For example, differences in the timing of breeding. Spizella taver- Curve-billed Thrashers (Toxostoma curvirostre) have neri does not return to the breeding grounds until 4± been divided into two morphologically distinct sub- 6 weeks after S. breweri has begun nesting, reducing species clusters (the Curvirostre and Palmeri groups) the likelihood of interbreeding. Mayr and Johnson also that correspond to an east-west division in southwest- emphasized the lack of information on pairing behav- ern North America, yet seven subspecies are generally ior of the two taxa. In particular, they focused on our accepted. Recent morphometric (Rojas-Soto 1998) and discussion of the differing vocal characteristics. Al- mtDNA analyses (Zink and Blackwell-Rago 2000) though differences in advertising song might or might support division into only two (or possibly three) evo- not be important in assessing reproductive isolation lutionary units, which we consider species. Indeed, a among allopatric populations (McKitrick and Zink loss of information occurs when all 7 subspecies are 1988), the vocal differences are more convincing than given equal rank. Similarly inappropriate is the clas- Mayr and Johnson suggest. Spizella taverneri songs si®cation of S. taverneri as a subspecies. from populations separated by thousands of kilometers The principle of balance. Nothing in the formal tax- are more similar to each other than they are to S. bre- onomic code mandates that taxonomists follow this so- weri songs of only a few hundred kilometers away. called ``principle'' of balance. Classi®cations are sys- Misinterpretation of individual variation as represen- tems for the storage and retrieval of information (al- tative of population-level differences would not pro- though the nature of this is under debate, Withgott duce this pattern. Nevertheless, we agree that taken 2000), but this information should reveal evolutionary alone, the vocal evidence is insuf®cient for establish- patterns, not degrees of sequence divergence. Spizella ing unambiguously the species status of taverneri (a taverneri need not be as different from S. breweri as comprehensive geographic survey is needed). S. breweri is from other congeners. In fact, we know We concluded that the combined vocal, morpholog- of no molecular studies that ®nd all congeners equally ical, behavioral, and ecological evidence presented is related, including the genus Vireo, which Mayr and consistent with the genetic evidence in suggesting that Johnson discuss. Mayr and Johnson's implication that Spizella breweri and S. taverneri are on independent congeners should be morphologically and genetically evolutionary trajectories. We believe that using these equidistant (a ``star phylogeny'') is inconsistent with combined sources of evidence to assess taxonomic the way we understand evolution to occur; some spe- rank is preferable to inferring reproductive isolation cies (within a clade) are older than others. Evolution among allopatric populations. The most appropriate need not produce balanced clades, and classi®cations hypothesis, when the facts (including eight years of should not be constructed to make them so. The clas- ®eld experience with these birds) are considered, is si®cation of Spizella should convey that S. taverneri that taverneri is both a phylogenetic and a biological and S. breweri are sister species. Reference to the orig- species. inal paper (Klicka et al. 1999) will show interested Information. According to Mayr and Johnson, in- readers the degree of sequence differentiation. formation is lost if S. taverneri is elevated to species When does a species become a species? At the cen- level. Using similar logic, we suggest that more im- ter of the current discussion is identifying the point in portant information is lost by not elevating S. taverneri the process of evolutionary divergence at which an to species status, namely that S. taverneri and S. bre- isolated taxon becomes a species (Avise and Walker weri are independently evolving units. Ranking very 1998). Klicka and Zink (1999) reviewed the stages that closely related (i.e., young) taxa as species is standard occur when a single population is divided into two in classi®cations, and few seem to be perplexed with daughter lineages. For a considerable period, mtDNA questions concerning sister relationships and allopatry. haplotypes are paraphyletic with respect to the splitting Established procedures (Nelson and Platnick 1981) for of the lineage; this is partly true in the present discus- translating a phylogeny into a classi®cation would con- sion, as the haplotype identifying S. taverneri is em- vey the fact that S. breweri and S. taverneri are sister bedded within the clade belonging to S. breweri (Klic- species; however, such information is often lost in avi- ka et al. 1999). After approximately 4Ne generations an classi®cations (Barrowclough and Cracraft 1984). of isolation, the mtDNA haplotype tree is reciprocally The notion that information about the allopatry of S. monophyletic (membership in either daughter species breweri and S. taverneri is lost by making them sep- is unambiguous based on DNA). Because haplotypes arate species is irrelevant because classi®cations are representing S. breweri and S. taverneri are not mu- not intended to reveal geographic distributions. tually reciprocally monophyletic, we believe that the A second problem with their argument involves the speciation event was very recent. How we recognize taxonomic inconsistency of subspecies. The position species depends on the species concept employed. At 422 COMMENTARY

the point of reciprocal monophyly, one could consider SON. In press. A cytochrome-b perspective on Pas- the two lineages to be phylogenetic (and evolutionary) serina bunting relationships. Auk. species. More divergence (anagenesis) typically must KLICKA, J., AND R. M. ZINK. 1999. Pleistocene effects occur before the lineages are reproductively isolated on North American songbird evolution. Proceed- and subsequently recognized by taxonomists as bio- ings of the Royal Society of London Series B 266: logical species (Avise and Walker 1998). Even after 695±700. this time, species can continue to diverge without sub- KLICKA, J., R. M. ZINK,J.C.BARLOW,W.B.MCGIL- sequent splitting. Hence, ``species'' of whatever ilk can LIVRAY, AND T. J. DOYLE. 1999. Evidence sup- be very similar or very different from congeners as a porting the recent origin and species status of the logical consequence of the evolutionary process. Timberline Sparrow. Condor 101:577±588. Spizella taverneri represents a very young species, MAYR, E., AND P. D. ASHLOCK. 1991. Principles of sys- displaying precisely the morphological and genetic tematic zoology. 2nd ed. McGraw Hill, Inc., New characteristics we would expect to see in a newly York. evolved species. Indeed, we think it is one of the most MAYR, E., AND N. K. JOHNSON. 2001. Is Spizella ta- likely examples of a Late Pleistocene speciation event verneri a species or a subspecies? Condor 103: 418±419. in a North American bird (Klicka and Zink 1999). MCKITRICK, M. C., AND R. M. ZINK. 1988. Species Mayr and Johnson, following the BSC, would prefer concepts in ornithology. Condor 90:1±14. to wait until there is evidence that the independent NELSON, G., AND N. PLATNICK. 1981. Systematics and evolutionary trajectories of S. taverneri and S. breweri biogeography. Columbia University Press, New are irreversible. We believe that the preponderance of York. the evidence suggests that S. taverneri is evolving in- PETERSON,A.T.,AND A. G. NAVARRO-SIGUÈ ENZA. 1999. dependently, and that recognition of this independence Alternate species concepts as bases for determin- is more important than burying it at the subspeci®c ing priority conservation areas. Conservation Bi- level. The philosophical underpinnings of alternative ology 13:427±431. species concepts allow for multiple interpretations of ROJAS-SOTO, O. 1998. VariacioÂn geogra®ca de las po- the same evidence. In paticular, reducing S. taverneri blaciones de Toxostoma curvirostre (Mimidae) de to a subspecies reveals the problems inherent in de- las zonas aridas de NorteameÂrica. M.Sc. thesis, scribing patterns of biodiversity when following the Universidad Nacional Autonoma de Mexico, D. F. BSC (Peterson and Navarro-SiguÈenza 1999). MeÂxico, MeÂxico. We thank R. Holzenthal for helpful discussion and WHEELER, Q. D., AND R. MEIER. 2000. Species con- Adolfo Navarro for translating the abstract into Span- cepts and phylogenetic theory. Columbia Univer- ish. sity Press, New York. WITHGOTT, J. 2000. Is it ``So long, Linnaeus?'' Bio- LITERATURE CITED science 50:646±651. ZINK, R. M., G. F. BARROWCLOUGH,J.L.ATWOOD, AND R. C. BLACKWELL-RAGO. 2000. Genetics, taxono- AVISE,J.C.,AND D. WALKER. 1998. Pleistocene phylo- geographic effects on avian populations and the my and conservation of the threatened California Gnatcatcher. Conservation Biology 14:1394± speciation process. Proceedings of the Royal So- 1405. ciety of London Series B 265:457±463. ZINK, R. M., AND R. C. BLACKWELL-RAGO. 2000. Spe- BARROWCLOUGH,G.F.,AND J. CRACRAFT. 1984. {un- cies limits and recent population history in the titled review} Check-list of North American birds. Curve-Billed Thrasher. Condor 102:881±886. Sixth Ed. Auk 101:628±632. ZINK, R. M., AND J. I. DAVIS. 1999. New perspectives GUTIE RREZ, R. J., G. F. BARROWCLOUGH, AND J. G. on the nature of species. Proceedings of the Inter- GROTH. 2000. A classi®cation of the grouse (Aves: national Ornithological Congress 22:1505±1516. Tetraoninae) based on mitochondrial DNA se- ZINK, R. M., AND M. C. MCKITRICK. 1995. The debate quences. Wildlife Biology 6:205±211. about species concepts and its implications for or- KLICKA, J., A. J. FRY,R.M.ZINK, AND C. W. THOMP- nithology. Auk 112:701±719.