Isolating barriers and microevolution in sympatric populations of the blackcap (Sylvia atricapilla)

• Antragsteller: Privatdozent Dr. H. Martin Schaefer
• Fachliche Zuordnung: Evolutionäre Zell- und Entwicklungsbiologie der Tiere
• Förderung: Förderung von 2009 bis 2013
• Projektkennung: Deutsche Forschungsgemeinschaft (DFG) - Projektnummer 133162540

• Erstellungsjahr: 2014

Zusammenfassung der Projektergebnisse

The most significant finding was our report that sympatric blackcap (Sylvia atricapilla) populations differing in their migratory route show slight, but significant phenotypic and genetic differentiation in neutral markers, and that this differentiation exceeds that of allopatric populations with the same migratory route. In total five morphological traits differed between birds following distinct migratory routes. Differentiation in wing shape and beak shape are most likely attributable to distinct selection regimes associated with the two migratory routes. Variation in migratory behaviour can thus lead to multifarious selection regimes that stimulate the evolution of distinct ecotypes. This work published in Current Biology stimulated wide interest in the public media because it supports rapid, contemporary evolution of reproductive isolation in sympatry suggesting that migratory routes can have strong impact on population differentiation. It was featured by Financial Times, American Scientist, Times, National Public Radio (http://www.npr.org/templates/story/story.php?storyId=121092289), and many others. After we found the divergence of populations following distinct migratory routes, we investigated the mechanisms underlying this divergence. We initially hypothesised that the divergence is caused by founder effects. We later corroborated that hypothesis owing to three facts. First, the large genetic distances among NW migrants suggest multiple founder effects. Second, our comparison on the population genetics of twelve European blackcap populations suggest that the microevolutionary shift in migratory behaviour indeed occurred in populations of SW migrants close the old SW/SE migratory divide. Third, a lack of genetic divergence across the SW/SE migratory divide in blackcaps shows substantial gene flow despite distinct migratory routes. Thus, distinct migratory routes do not necessarily disrupt gene flow. As a next step we showed that temporal and spatial isolation among SW and NW migrating blackcaps in sympatry contribute to maintain the genetic divergence attributed to founder effects. Using null models we revealed that temporal isolation alone leads to 30% reproductive isolation of NW migrants. These null models do not account for the fact that early arriving blackcaps are in better physical condition and genetic constitution than later arriving blackcaps. Thus, early arriving migrants, in which NW migrating birds are overrepresented, are likely to have a larger fitness than later arriving blackcaps. This could partially explain the growth of the proportion of NW migrating birds over the last decades. In sum, we could show that at least two isolating barriers are acting in sympatric blackcap populations reducing gene flow among them. We showed that the two distinct migratory routes of blackcaps in SW Germany did not result in distinct Haemosporidian parasites. Blackcaps infected with Haemosporidians remain so for life. Haemoproteus parabelopolskyi had a marginal effect on arrival dates of blackcaps. The corresponding article was selected as Editor’s Choice reflecting their assessment of this paper as a particularly important one. Thus, our results suggest that the distinct selection regimes associated to the NW and SW migratory route do not include Haemosporidian parasites. Based on this project, we propose that the evolution of migratory ecotypes is a subtle but potentially widespread process that improves adaptive responses toward the diverse ecological settings that migrants experience.

Projektbezogene Publikationen (Auswahl)

• 2009: A recent migratory divide facilitates the contemporary evolution of reproductive isolation and phenotypic divergence in sympatry. Current Biology 19: 2097-2101
  Rolshausen G., Segelbacher, G., Hobson K. & H. M. Schaefer
  
• 2010: Spring arrival along a migratory divide of sympatric blackcaps (Sylvia atricapilla). Oecologia 162: 175-183
  Rolshausen, G., K. Hobson & H. M. Schaefer
  
• 2011: Diversity of avian haemosporidians along a recently evolved migratory divide. Parasitology 138: 824-835
  Santiago-Alarcon, D., Bloch, R., Rolshausen, G. Schaefer, H. M. & G. Segelbacher
  
• 2012: Diptera vectors of avian haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews 87: 928-964
  Santiago-Alarcon, D., Valkiunas, V. & H. M. Schaefer
  
• 2013: Contrasting patterns of genetic differentiation among Blackcaps (Sylvia atricapilla) with divergent migratory orientations in Europe. PloS One e81365
  Mettler, R., Schaefer H.M., Chernetsov, N., Fiedler, W., Hobson, K.A., Ilieva, M., Imhof, E., Johnsen, A., Renner, S.C., Rolshausen, G., Serrano, D., Wesolowski, T. & G. Segelbacher
  
• 2013: Development of nine microsatellite marker in a migratory songbird, the blackcap (Sylvia atricapilla). Molecular Ecology Resources 13: 341-343
  Molecular Ecology Resources Primer Consortium
  
• 2013: Haemosporidian parasitism in the blackcap (Sylvia atricapilla) in relation to spring arrival date and body condition. Journal of Avian Biology 44: 521-530
  Santiago-Alarcon, D., Mettler, R., Segelbacher G & H. M. Schaefer
  
• 2013: Individual differences in migratory behaviour shape population genetic structure and microhabitat choice in sympatric blackcaps (Sylvia atricapilla). Ecology and Evolution 3 : 4278-4289
  Rolshausen G., Segelbacher, G., Hermes C., Hobson K. & H. M. Schaefer