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Species Limits and Biogeography of Rhynchospiza Sparrows

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Species Limits and Biogeography of Rhynchospiza Sparrows Journal of Ornithology (2019) 160:973–991 https://doi.org/10.1007/s10336-019-01695-2 ORIGINAL ARTICLE Species limits and biogeography of Rhynchospiza sparrows Juan I. Areta1 · Emiliano A. Depino1 · Sergio A. Salvador2 · Steven W. Cardif3 · Kevin Epperly4 · Ingrid Holzmann1 Received: 17 April 2019 / Revised: 7 July 2019 / Accepted: 18 July 2019 / Published online: 6 August 2019 © Deutsche Ornithologen-Gesellschaft e.V. 2019 Abstract The genus Rhynchospiza comprises two species, the monotypic Tumbes Sparrow (R. stolzmanni) and the Stripe-crowned Sparrow (R. strigiceps) with subspecies strigiceps and dabbenei. In the study reported here we evaluated the taxonomic status of these taxa and discussed key features involved in speciation. All three taxa exhibited multiple diferences in plum- age, morphology, and vocalizations, supporting the recognition of three species in Rhynchospiza. The very large-billed R. stolzmanni has a song composed of a succession of faster complex trilled phrases, shows a small black loral line and dark- chestnut head stripes with large dark central-stripe to individual feathers, and is resident in the Tumbes region. The large and heavy dabbenei has a song consisting of a series of simple chirping notes, shows a large black loral crescent and chestnut head stripes with a reduced to absent dark center to feathers, and inhabits the Austral Yungas as a year-round resident. The small and pale strigiceps has a song consisting of a succession of complex trilled phrases, shows a small black loral line and rufous-brown head stripes with large dark central-stripe to feathers, and inhabits Dry and Sierran Chaco where it is a partial migrant. Locality data and ecological niche modeling show that dabbenei and strigiceps are allo-parapatric and use diferent altitudinally segregated habitats at their zone of parapatry. Molecular phylogenetic analyses (NADH dehydrogenase 2 [ND2] gene) revealed R. stolzmanni to be sister (11.5% divergent) to a recently diverged dabbenei and strigiceps clade (1.6% divergent). We conclude that the genus Rhynchospiza comprises three species-level entities, each restricted to a major biogeographic region, and that vocalizations and facial patterns provide key evidence on species limits in these otherwise similarly plumaged taxa. The evolutionary–cultural diferences in songs, with complex phrases in those of R. strigiceps and R. stolzmanni, and single notes in the songs of R. dabbenei, suggest changes in the innate vocal learning template during speciation in the latter. Keywords Neotropical birds · Plumage conservatism · Speciation · Specifc mate recognition systems · Vocal template Zusammenfassung Artabgrenzung und Biogeographie der Neuweltammer-Gattung Rhynchospiza Die Gattung Rhynchospiza umfasst zwei Arten, die monotypische Tumbesammer (R. stolzmanni) und die Streifenscheitelammer (R. strigiceps) mit den Unterarten strigiceps und dabbenei. Wir beurteilen hier den taxonomischen Status und diskutieren die Schlüsselmerkmale der Artbildung. Alle drei Taxa zeigten zahlreiche Unterschiede im Gefeder, in der Morphologie und der Communicated by J. T. Lifeld. Deceased: Sergio A. Salvador. Electronic supplementary material The online version of this article (https ://doi.org/10.1007/s1033 6-019-01695 -2) contains supplementary material, which is available to authorized users. * Juan I. Areta 2 Villa María, Córdoba, Argentina [email protected] 3 Museum of Natural Science, Louisiana State University, Baton Rouge, LA, USA 1 Instituto de Bio y Geociencias del Noroeste Argentino (IBIGEO-CONICET), Laboratorio de Ecología, 4 Burke Museum of Natural History and Culture Comportamiento y Sonidos Naturales (ECOSON), and Department of Biology, University of Washington, Rosario de Lerma, Salta, Argentina Seattle, WA, USA Vol.:(0123456789)1 3 974 Journal of Ornithology (2019) 160:973–991 Lautäußerung, was die Unterscheidung der drei Arten in der Gattung Rhynchospiza unterstützt. Die Art R. stolzmanni besitzt einen kräftigen Schnabel, hat einen Gesang zusammengesetzt aus einer Abfolge von schnellen, komplexen Triller-Phrasen, weist einen schmalen schwarzen Zügelstreifen und einen kastanienbraun gefärbten Scheitelseitenstreifen mit einzelnen Federn auf, die breite dunkle Federzentren besitzen, und sie ist in der Tumbes-Region (Peru) heimisch. Die große und schwere Unterart dabbenei besitzt einen Gesang aus einer Serie von einfachen Tschilp-Elemente, einen großen schwarzen, halbmondförmigen Zügelstreifen, rotbraun gefärbte Scheitelseitenstreifen, deren Federn nur schwache bis fehlende dunkle Federzentren aufweisen, und sie bewohnt den südlichen Yungas (Region in Bolivien) als Jahresvogel. Die kleine und blass gefärbte Unterart strigiceps besitzt einen Gesang zusammengesetzt aus einer Abfolge an komplexen Triller-Phrasen, hat einen kleinen schwarzen Zügelstreifen, rötlichbraune Scheitelseitenstreifen mit Federn mit großen dunklen Federzentren und lebt in „Dry Chaco“und „Sierra Chaco“als Teilzieher. Verbreitungsdaten und ökologische Nischenmodellierungen zeigen, dass die Unterarten dabbenei und strigiceps allo-parapatrisch sind und aufgrund unterschiedlicher Höhenlagen getrennte Habitate ihres parapatrischen Verbreitungsgebiets nutzen. Molekularphylogenetische Analysen (ND2 Gene) haben gezeigt, dass R. stolzmanni eine Schwesterart (11.5% Divergenz) der jüngst aufgespaltenen Klade dabbenei und strigiceps (1.6% Divergenz) ist. Wir folgern daraus, dass die Gattung Rhynchospiza drei Einheiten auf Artniveau umfasst, jede davon beschränkt auf eine große biogeographische Region. Die Lautäußerungen und Kopfzeichnungen bieten Schlüsselmerkmale zur Artenabgrenzung in diesem, ansonsten ähnlich gefederten Taxa. Die evolutionskulturellen Unterschiede im Gesang, die komplexen Phrasen in R. strigiceps und R. stolzmanni sowie die Einzelsilben in R. dabbenei weisen darauf hin, dass bei Letzterer Änderungen in den angeborenen Gesangslernmustern während der Artbildung entstanden sind. Introduction it is embedded, coupled to the many possible levels of change, lead to the existence of a large number of types Understanding how long-term ecological and geographic of mating groups. The diversity of mating recognition barriers have acted to create biogeographic patterns requires systems includes mating groups that difer in many traits knowledge on the spatial distribution of phenotypes, the key to mate recognition (Zimmer and Whittaker 2000; level of diference between them, and what these difer- Jordan et al. 2018), cryptic species that cannot be safely ences entail from the perspective of facilitating or restrict- distinguished based on external features but instead dif- ing free interbreeding. Characterizing the multidimensional fer in vocalizations (Stein 1958; Ábalos and Areta 2009), phenotypes of populations and assessing the extent of their populations that difer in vocalizations but that seem to be abilities to interbreed remain key endeavors of the study of otherwise identical in plumage and morphology (Schwartz biodiversity. Studies on species limits that provide natural 1975; Areta and Repenning 2011; Areta 2012), the exist- history, morphological, and distributional data and informa- ence of morphs that difer markedly in plumage but appear tion on characters thought to be important in mate choice to interbreed freely (Areta 2008; Areta et al. 2011; Chavar- are paramount to the goal of understanding the origin, dif- ría-Pizarro et al. 2010) or not so freely (Pryke and Grifths ferentiation, and maintenance of lineages. 2009; Falls and Kopachena 2010), taxa with gene fow In birds, an immense array of signaling systems is used in wide or narrow contact zones (Fernando et al. 2016; for mating. Changes in these systems result in the appear- Areta et al. 2017), and the disputed “ring species” or Ras- ance and maintenance of diferent mating groups. Within senkreis (Irwin et al. 2001; Liebers et al. 2004; Alcaide each of these mating groups, genetic recombination is et al. 2014), among other possibilities. This very diversity mediated by a mate recognition system that leads to the and the relational value of mating character changes imply long-term maintenance of the respective groups (Paterson that any search for a generalized quantitative species-level 1980, 1985; Coyne and Orr 2004; Price 2008). Mate rec- threshold is doomed to fail (Tobias et al. 2010; Remsen ognition systems refect the variable emphasis of diferent 2015, 2016; Collar et al. 2016) because no single con- suites of characters, with some systems depending heavily cept or a single taxonomic category can accommodate all on visual cues, others relying more on vocal cues, and still this variation while keeping its explanatory power. Thus, other systems requiring multimodal signaling for proper a more fruitful research program would be to focus on functioning (Bradbury and Vehrencamp 1998; Price 2008). understanding how diferent levels of change in diferent Thus, changes of a certain magnitude in a signaling feature idiosyncratic suites of characters evolve to form coherent cannot be assumed to have a universal efect in all systems. signaling systems that result in complete or partial assorta- Instead, changes of the same magnitude may have drastic tive mating in diferent taxonomic groups. efects in one system but virtually no efect in another. The conservative plumages of “striped-sparrows” in This relative or context-dependent efect of the change the speciose genus Aimophila have resulted in difculties of a feature operating within the mating system in which clarifying
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