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Speciation Associated with Shifts in Migratory Behavior in an Avian Radiation

2020; Elsevier BV; Volume: 30; Issue: 7 Linguagem: Inglês

10.1016/j.cub.2020.01.064

1879-0445

Valentina Gómez‐Bahamón, Roberto Márquez, Alex E. Jahn, Cristina Yumi Miyaki, Diego T. Tuero, Oscar Laverde-R., Silvia Restrepo, Carlos Daniel Cadena,

Ecology and Vegetation Dynamics Studies

Migratory animals move up to thousands of kilometers every year [1Dingle H. Migration: The Biology of Life on the Move. Oxford University Press, 1996Google Scholar]. Losses of migration (i.e., migratory drop-offs) occur when individuals of a migratory species stop migrating and establish founder sedentary populations, a phenomenon documented in birds [2Winger B.M. Lovette I.J. Winkler D.W. Ancestry and evolution of seasonal migration in the Parulidae.Proc. Biol. Sci. 2012; 279: 610-618Crossref PubMed Scopus (27) Google Scholar, 3Winger B.M. Barker F.K. Ree R.H. Temperate origins of long-distance seasonal migration in New World songbirds.Proc. Natl. Acad. Sci. USA. 2014; 111: 12115-12120Crossref PubMed Scopus (35) Google Scholar, 4Rolland J. Jiguet F. Jønsson K.A. Condamine F.L. Morlon H. Settling down of seasonal migrants promotes bird diversification.Proc. Biol. Sci. 2014; 281: 20140473Crossref PubMed Scopus (40) Google Scholar, 5Dufour P. Descamps S. Chantepie S. Renaud J. Guéguen M. Schiffers K. Thuiller W. Lavergne S. Reconstructing the geographic and climatic origins of long‐distance bird migrations.J. Biogeographr. 2020; 47: 155-166Crossref Scopus (0) Google Scholar] and butterflies [6Zhan S. Zhang W. Niitepõld K. Hsu J. Haeger J.F. Zalucki M.P. Altizer S. de Roode J.C. Reppert S.M. Kronforst M.R. The genetics of monarch butterfly migration and warning colouration.Nature. 2014; 514: 317-321Crossref PubMed Scopus (70) Google Scholar]. In theory, losses—and also gains—of migration might promote speciation if sedentary and migratory populations become reproductively isolated [7West-Eberhard M.J. Developmental Plasticity and Evolution. Oxford University Press, 2003Crossref Google Scholar, 8Winker K. On the origin of species through heteropatric differentiation: a review and a model of speciation in migratory animals.Ornithol. Monogr. 2010; 69: 1-30Crossref Google Scholar, 9Price T. Speciation in Birds. Roberts and Company, 2008Google Scholar]. Because migratory and sedentary strategies involve alternative physiological, behavioral, and morphological traits [10Alerstam T. Hedenström A. Akesson S. Long-distance migration: evolution and determinants.Oikos. 2003; 103: 247-260Crossref Scopus (613) Google Scholar, 11Berthold P. Bird Migration: A General Survey. Oxford University Press, 2001Google Scholar, 12Zink R.M. Towards a framework for understanding the evolution of avian migration.J. Avian Biol. 2002; 33: 433-436Crossref Scopus (46) Google Scholar, 13Taylor R.S. Friesen V.L. The role of allochrony in speciation.Mol. Ecol. 2017; 26: 3330-3342Crossref PubMed Scopus (35) Google Scholar], divergence along multiple axes of organismal function is expected to accompany switches in migratory behavior, potentially accelerating speciation. We present evidence of speciation driven by a migratory drop-off in the fork-tailed flycatcher (Tyrannus savana) resulting in reproductive isolation likely driven by changes in breeding schedules (allochronic speciation [13Taylor R.S. Friesen V.L. The role of allochrony in speciation.Mol. Ecol. 2017; 26: 3330-3342Crossref PubMed Scopus (35) Google Scholar, 14Quintero I. González-Caro S. Zalamea P.-C. Cadena C.D. Asynchrony of seasons: genetic differentiation associated with geographic variation in climatic seasonality and reproductive phenology.Am. Nat. 2014; 184: 352-363Crossref PubMed Scopus (10) Google Scholar, 15Bearhop S. Fiedler W. Furness R.W. Votier S.C. Waldron S. Newton J. Bowen G.J. Berthold P. Farnsworth K. Assortative mating as a mechanism for rapid evolution of a migratory divide.Science. 2005; 310: 502-504Crossref PubMed Scopus (276) Google Scholar]) and geographic isolation of breeding grounds (allopatric speciation [16Mayr E. Systematics and the Origin of Species. Columbia University Press, 1942Google Scholar]). Phylogenetic analyses across New World flycatchers (Tyrannidae) showed that an association between speciation and drop-offs is also observable at a macroevolutionary scale. Loss of migration was significantly more frequent than its gain, and speciation rates of migratory and partially migratory lineages (i.e., species having both migratory and sedentary populations) exceeded those of sedentary lineages. Models of trait evolution indicated that partial migration is an intermediate step between migratory and sedentary states in this family. Given that partial migration is widespread across migratory animals (e.g., of all migratory birds, ca. 51% are partially migratory [5Dufour P. Descamps S. Chantepie S. Renaud J. Guéguen M. Schiffers K. Thuiller W. Lavergne S. Reconstructing the geographic and climatic origins of long‐distance bird migrations.J. Biogeographr. 2020; 47: 155-166Crossref Scopus (0) Google Scholar]), speciation via switches in migratory behavior might be an important yet overlooked mechanism of animal diversification.