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Phylogeny, Historical Biogeography and the Evolution of Migration in Accipitrid Birds of Prey (Aves: Accipitriformes)

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Phylogeny, Historical Biogeography and the Evolution of Migration in Accipitrid Birds of Prey (Aves: Accipitriformes) Ornis Hungarica 2014. 22(1): 15–35. DOI: 10.2478/orhu-2014-0008 Phylogeny, historical biogeography and the evolution of migration in accipitrid birds of prey (Aves: Accipitriformes) Jenő nagy1 & Jácint tökölyi2* Jenő Nagy & Jácint Tökölyi 2014. Phylogeny, historical biogeography and the evolution of mig ration in accipitrid birds of prey (Aves: Accipitriformes). – Ornis Hungarica 22(1): 15–35. Abstract Migration plays a fundamental part in the life of most temperate bird species. The re­ gu lar, large­scale seasonal movements that characterize temperate migration systems appear to have originated in parallel with the postglacial northern expansion of tropical species. Migratoriness is also in- fluenced by a number of ecological factors, such as the ability to survive harsh winters. Hence, understanding the origins and evolution of migration requires integration of the biogeographic history and ecology of birds in a phylogenetic context. We used molecular dating and ancestral state reconstruction to infer the origins and evolu- tionary changes in migratory behavior and ancestral area reconstruction to investigate historical patterns of range evolution in accipitrid birds of prey (Accipitriformes). Migration evolved multiple times in birds of prey, the ear- liest of which occurred in true hawks (Accipitrinae), during the middle Miocene period, according to our analy- ses. In most cases, a tropical ancestral distribution was inferred for the non­migratory ancestors of migratory line- ages. Results from directional evolutionary tests indicate that migration evolved in the tropics and then increased the rate of colonization of temperate habitats, suggesting that temperate species might be descendants of tropi- cal ones that dispersed into these seasonal habitats. Finally, we found that diet generalization predicts migratori- ness in this group. Keywords: ancestral area reconstruction, annual cycle, comparative, diet specialization, diurnal birds of prey, mo- lecular dating, seasonality Összefoglalás A legtöbb mérsékelt övi madárfaj életciklusában alapvető szerepet tölt be a vonulás. A rendszeres, nagy kiterjedésű mozgások, melyek a mérsékelt övi vonulási rendszereket jellemzik, egyes feltételezések szerint a trópusi fajok poszt­glaciális, északi irányú terjeszkedésével párhuzamosan jelentek meg. Ezen felül a vonulás előfordulását számos ökológiai tényező is befolyásolhatja, mint például a környezet szezonalitásának mértéke vagy a téli túlélést befolyásoló tényezők. A vonulás eredete és evolúciója ezért csak úgy érthető meg, ha a madarak biogeográfiai törté- netiségét és ökológiáját filogenetikai kontextusban tanulmányozzuk. Jelen vizsgálatban a vágómadár­alakúak (Acci- pitriformes) vonulásának evolúcióját elemeztük komparatív módszerekkel. Első lépésben létrehoztunk egy fosszilis adatok alapján datált molekuláris törzsfát, amelyen jellegrekonstrukciót végeztünk és rekonstruáltuk a fajok ősi elter- jedési területét. Az elemzéseink alapján a vonulás többször alakult ki a ragadozók esetében, legkorábban a héjafor- mákon (Accipitrinae) belül, vélhetően a Miocén közepén. A legtöbb esetben a vonuló leszármazási vonalak nem vo- nuló őseinél trópusi elterjedésre következtethetünk. A direkcionális evolúciós teszt alapján a vonulás a trópusokon jelent meg és megnövelte a mérsékelt égöv kolonizációjának rátáját. Eszerint tehát a mérsékelt övi ragadozómadár fa- jok vonuló trópusi fajok leszármazottainak tekinthetők, melyek az erősen szezonális, északi élőhelyek irányába ter- jeszkedtek. Végezetül negatív kapcsolatot találtunk a vonulás megjelenése és a táplálékspecializáció mértéke között. Kulcsszavak: éves ciklus, jellegrekonstrukció, komparatív, molekuláris datálás, nappali ragadozómadarak, sze- zonalitás, táplálékspecializáció 1 MTA-ELTE-MTM Ecology Research Group, 1117 Budapest, Pázmány Péter sétány 1/C, Hungary, e-mail: jenon- [email protected] 2 MTA-DE “Lendület” Behavioural Ecology Research Group, Department of Evolutionary Zoology and Human Biology, University of Debrecen, 4032 Debrecen, Egyetem tér 1., Hungary, [email protected] *corresponding author Brought to you by | Swinburne Technical University Authenticated Download Date | 12/29/14 2:10 PM 16 ORNIS HUNGARICA 2014. 22(1) Introduction migratory restlessness (‘zugunruhe’) during the annual cycle and (3) a range of physio- Birds originated, according to our current logical adaptations that cover the metabolic knowledge of the fossil record, about 150­ requirements of long­distance flights during 200 million years ago during the geologi- migration. Understanding how such a comp­ cal era of Jurassic (Padian & Chiappe 1998). lex phenotype could have evolved is a major The appearance of powered flight, probab­ challenge in ornithology. ly in combination with several other avi- While a wealth of information has accu- an fea tures such as warm­bloodedness and mulated on the details of the process of mig­ the presence of extensive parental care has ration, comparatively little is known about fuelled the diversification of this group of how migration originated and evolved in vertebrates, which seems to have accele­ birds. This is not surprising, since behavio- rated around, or shortly after the Cretaceous­ ral traits, such as the migratory habits of a Pa leo gene boundary (Ericson et al. 2006, species do not fossilize and hence our cur- Brown et al. 2008, Jetz et al. 2012). rent ideas of it are strictly inferred from The widespread occurrence of birds is phylogenetic or biogeographic studies. Cur- greatly facilitated by their excellent dis- rent theories of the evolution of migra- persal capabilities. This is perhaps most tion can be divided into two groups (Rap- clearly seen in migratory birds, which can pole & Jones 2002, Bruderer & Salewski travel thousands of kilometres on continen- 2008). The ‘tropical origin’ hypothesis pro- tal scale within a single year. Migration is poses that migratory birds derive from spe- a characteristic feature of birds that is ex- cies inhabiting regions where environmen- tremely common especially in species in- tal factors were constant during the year, habiting the Northern Hemisphere tempe­ so there was no need for migration. These rate zone and the Arctic, but it also occurs, species could have colonized more sea- although in less extreme forms, in other re- sonal, northern habitats, which, during the gions of the globe in the form of intratropi- summer months provided appropriate con- cal migration systems (Alerstam 1993, Ber­ ditions for reproduction. However, during thold 2001, Newton 2008). winter food availability decreased, hence Migration itself profoundly influences the these birds were forced to return to southern distribution, ecology and diversification of latitudes (Rappole & Jones 2002, Bruderer birds (Newton 2008), hence it is not surpri­ & Salewski 2008). Cox (1985) developed sing that a great deal of information has ac- a stepping­stone model of this hypothesis. cumulated on its internal, proximate deter- According to this model, resource­limita- minants and its phenology ever since Hans tion due to competition for food forced cer- Christian Mortensen started ringing birds at tain tropical resident species to expand their the very end of the 19th century. These studies range to the subtropics. These birds continu­ revealed that the migratory phenotype is de- ed to return to the tropics during the winter, termined by a set of complex and tightly re­ resulting in the formation of partial migrant gu lated mechanisms (Gwinner 1990), which species. These partial migrants then continu­ includes, among others (1) sensory elements ed to spread to higher latitudes where they underlying orientation and navigation, (2) were able to breed successfully while still mechanisms responsible for the regulation of returning to the original area in the winter Brought to you by | Swinburne Technical University Authenticated Download Date | 12/29/14 2:10 PM J. Nagy & J. Tökölyi 17 (Stiles 1980, Cox 1985). Thus, this hypo the­ evolution of migration by forcing non­mig­ sis predicts that migratory species evolved ratory temperate and arctic species to leave from tropical ancestors. there home ranges during the winter (Bell Several lines of evidence support the tro­ 2000, 2005), resulting in migratory strate- pi cal origin of long­distance migrants. Jo- gies which allowed the survival of popu- seph et al. (1999), in a study of waders, lations in a strongly seasonal milieu (Bell analyzed the evolution of breeding and win- 2000, 2005). Thus, this hypothesis predicts tering distribution of 16 species from the that migration evolved from temperate resi­ genus Charadrius using phylogenetic me­ dent species, a prediction that has received thods. By reconstructing the hypothesized relatively low support to date. It is clear, distribution of the ancestors of these birds, however, that migration can evolve with- they showed that species that are migratory out the expansion of the breeding ranges, today derive from ancestors whose breeding as examplified by the large number of in- and non­breeding ranges were located in the tra­tropical migrants (e.g. Boyle & Conway tropical zone. Another similar study inves- 2007, Boyle et al. 2011). Comparative stu­ tigated the evolution of migration in Ca- dies of the occurrence of migration among tharus thrushes (Outlaw et al. 2003). This some of these tropical taxa, such as the pas- study showed that North American (migra- serine group Tyranni revealed that a num- tory) thrushes are sister to tropical species, ber of
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