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Evolutionary Divergences in Luscinia Svecica Subspecies Complex – New Evidence Supporting the Uniqueness of the Iberian Bluethroat Breeding Populations

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Evolutionary Divergences in Luscinia Svecica Subspecies Complex – New Evidence Supporting the Uniqueness of the Iberian Bluethroat Breeding Populations Ornis Fennica 94: 141–149. 2017 Evolutionary divergences in Luscinia svecica subspecies complex – new evidence supporting the uniqueness of the Iberian bluethroat breeding populations Javier García*, Arild Johnsen, Benito Fuertes & Susana Suárez-Seoane J. García, S. Suárez-Seoane, Department of Biodiversity and Environmental Manage- ment, Faculty of Biological Sciences, University of León, Campus de Vegazana s/n, 24071 León, Spain. * Corresponding author’s e-mail: [email protected] B. Fuertes, Grupo Ibérico de Anillamiento. C/ Daoiz y Velarde, 16. 24006 León, Spain A. Johnsen, Natural History Museum, University of Oslo, PO Box 1172 Blindern, 0318 Oslo, Norway Received 12 August 2016, accepted 14 April 2017 The assessment of evolutionary divergences within subspecies complexes provide an ef- fective short-cut for estimating intraspecific genetic diversity, which is relevant for con- servation actions. We explore new evidence supplementing the existing knowledge about the singularity of Iberian bluethroats within the Luscinia svecica subspecies mosaic. We compared biometric traits of Iberian males (L. s. azuricollis) to the closest subspecies (L. s. cyanecula, L. s. namnetum and L. s. magna) using general linear models and analysed the correlations between biometric and genetic differentiation (based on nuclear micro- satellites) among the target subspecies with a Mantel test. Biometric differences were cal- culated using 63 museum skins and 63 live specimens. Genetic distances were estimated in a sample of 136 individuals. An additional characterisation of the plumage of Iberian males was shaped from 22 live specimens. We highlight the distinctiveness of Iberian birds within the subspecies mosaic since L. s. azuricollis had longer wings than L. s. cyanecula and L. s. namnetum, but shorter wings than L. s. magna. Indeed,L.s.azuricollis had longer tarsus and bill than L. s. namnetum, but shorter bill than L. s. magna. Biometric divergence was not significantly associated with genetic distance. Iberian males showed an all-blue plastron in 77% of specimens, a mostly non-marked black band and no white band, which distinguished them from males of L. s. cyanecula and L. s. namnetum.We conclude the importance of considering phenotypic and genotypic differences at subspe- cies level, which is essential for designing realistic conservation strategies addressed to preserve species genetic diversity patterns. 1. Introduction like the Nature 2000 network in Europe. However, conservation strategies may benefit from targeting The presence of endangered species is currently lower taxonomic levels of assessment to avoid one of the main principles for establishing priori- widespread loss of genetic diversity (Meffe & ties of conservation and designing protected areas, Carrol 1997). Successful conservation policies 142 ORNIS FENNICA Vol. 94, 2017 should be explicitly focused on the preservation of cies classification, neither about phylogenetic re- multiple populations across the range of the spe- lationships (Questiau et al. 1998, Eybert et al. cies, that should be self-sustaining, healthy and ge- 2003, Zink et al. 2003, Johnsen et al. 2006). netically robust (Redford et al. 2011), since ge- AccordingtoZinket al. (2003), only two netic variability determines the adaptive potential clades can be differentiated in Eurasia based on of the species and their resilience to environmental mitochondrial DNA studies. One of these groups changes (Reed & Frankham 2003). is located in northern Eurasia and includes chest- In the case of bird species, the assessment of nut-spotted subspecies (L. s. svecica, L. s. volgae intra-specific variation has been traditionally ad- and L. s. pallidogularis). The other comprises dressed at the taxonomic category of subspecies southern subspecies with or without a white throat (Winker 2010). The evaluation of bird subspecies spot (L. s. azuricollis, L. s. namnetum, L. s. cyane- is critical since it contributes to explain the current cula and L. s magna). Johnsen et al. (2006) found distribution and the biogeographic history of spe- evidence for low gene flow among northern and cies (Newton 2003). Indeed, according to Philli- southern groups, the latter being more differenti- more & Owens (2006), it offers an effective short- ated than the former. These authors also showed cut for estimating patterns of intraspecific genetic that Bluethroat genetic structure (based on micro- diversity, thereby providing a useful tool for the satellite marker analysis) was consistent with the study of evolutionary divergence and conserva- subspecies classification (based on phenotypic tion. However, it is important to have in mind that, features). They found significant qualitative varia- despite the convenience of using this study level, tion in throat spot coloration and quantitative vari- the traditional subspecies limits, that have been ation in hue, chroma and brightness of the UV/ based on phenotypic features, could sometimes be blue throat coloration that possibly evolved by contradicted by the outcomes derived from mod- sexual selection through female choice, in turn ern molecular techniques (Zink et al. 2003, leading to subspecies diversification (Peiponen Rheindt et al. 2011), which makes the approach 1960, Andersson & Amundsen 1997, Johnsen et more challenging. al. 1998, 2001). The bluethroat (Luscinia svecica) is a small Indeed, Hogner et al. (2013), on the basis of migratory passerine (weight 14–20 g) with bree- sperm characteristics, showed a significant differ- ding populations distributed through the west and entiation between L. s. svecica, L. s. namnetum, L. north of the Western Paleartic (Cramp 1988, De- s. cyanecula and L. s. azuricollis that was consis- ment’ev & Gladkov 1968). It has been incorpo- tent with the findings of Johnsen et al. (2006) and, rated in the Annex I of the European Union’s Birds therefore, supported the status of these subspecies Directive (Directive 2009/147/CE) that includes as independent taxa. The high number of differ- the most endangered species of Europe. The spe- ences existing between subspecies and their geo- cies shows a high sexual dichromatism, which in- graphic isolation indicate that Bluethroats are cur- fluences inter and intrasexual communication. In rently in an advanced stage of the speciation pro- the case of males, throat and breast are dominated cess, when compared with other subspecies com- by a large patch of ultraviolet (UV)/blue plumage plexes (Johnsen et al. 2006). (with or without a central spot of white/chestnut Iberian breeding Bluethroats have been tradi- coloration) and a breast band of chestnut plumage tionally misclassified within one of the white- below. Females are highly variable in the extent of spotted subspecies, L. s. cyanecula (Cramp 1988, their throat coloration, from entirely drab to almost Del Hoyo et al. 2005), although decades ago other male-like (Cramp 1988, Amundsen et al. 1997). authors as Mayaud (1958) and Corley-Smith The phenotypic variation of Bluethroats consti- (1959) had highlighted that they presented suffi- tutes a complex mosaic associated to differences in cient plumage differences to be considered as a geographical morphs and life history. Ten subspe- different subspecies (L. s. azuricollis). Recently, cies have been described according to both male Johnsen et al. (2006, 2007) and Hogner et al. throat ornament and general plumage patterns (2013) have shown that Iberian populations are (Cramp 1988, Del Hoyo et al. 2005), although a genetically well defined, both in nuclear micro- unanimous consensus does not exist about subspe- satellites and mtDNA (but see Zink et al. 2003). In García et al.: Evolutionary divergences in Luscinia svecica subspecies complex 143 Fig. 1. Study area. A) Map of Eurasia showing the geo- graphic location where Bluethroat specimens from dif- ferent subspecies were captured. B) Breeding distribution of Bluethroat in Spain (10 × 10 km UTM squares; Martí & Del Moral, 2003) and sampling locali- ties. this sense, the accurate assessment of subspecies svecica subspecies complex. In particular, we eva- taxonomic position, as well as the full characteri- luated biometric differences of Iberian males (L. s. sation of phenotypic and genotypic distinctiveness azuricollis) against those of the closest subspecies, of subspecies, is essential for implementing ade- according to geographic (L. s. cyanecula and L. s. quate measures of conservation addressed to pro- namnetum) and plumage (L. s. magna) criteria, tect the Eurasian Bluethroats as a whole. and tested the correlation between biometric and The objective of this study was to add new evi- genetic differentiation among the target subspe- dence that supplements the existing knowledge cies. Additionally, we aimed to carry out a specific about the relevance and singularity of the Iberian characterisation of Iberian males according to breeding bluethroats in the context of the Luscinia their plumage. 144 ORNIS FENNICA Vol. 94, 2017 2. Material and methods collected in Spain between 1999 and 2002 (Fig. 1b). We evaluated the tone of the breast blue In order to evaluate the biometric differences plastron (light, intermediate or dark), the colour of among subspecies, we have considered three vari- the spot (white, chestnut or blue if it were absent) ables: wing chord length (± 0.5 mm), tarsus length, and the presence of black, white and chestnut (± 0.1 mm) and bill length (± 0.1 mm) (Svensson breast bands (absent, not marked, marked or very 1992). These data have been collected
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