The Mitogenome Relationships and Phylogeography of Barn Swallows (Hirundo rustica)

Author:

Lombardo Gianluca1ORCID,Rambaldi Migliore Nicola1ORCID,Colombo Giulia1ORCID,Capodiferro Marco Rosario1ORCID,Formenti Giulio2ORCID,Caprioli Manuela3,Moroni Elisabetta1,Caporali Leonardo4ORCID,Lancioni Hovirag5ORCID,Secomandi Simona6ORCID,Gallo Guido Roberto6ORCID,Costanzo Alessandra3ORCID,Romano Andrea3ORCID,Garofalo Maria7ORCID,Cereda Cristina7ORCID,Carelli Valerio48ORCID,Gillespie Lauren9ORCID,Liu Yang10ORCID,Kiat Yosef11ORCID,Marzal Alfonso12ORCID,López-Calderón Cosme13ORCID,Balbontín Javier14ORCID,Mousseau Timothy A.15ORCID,Matyjasiak Piotr16ORCID,Møller Anders Pape17ORCID,Semino Ornella1ORCID,Ambrosini Roberto3ORCID,Bonisoli-Alquati Andrea18ORCID,Rubolini Diego3ORCID,Ferretti Luca1ORCID,Achilli Alessandro1ORCID,Gianfranceschi Luca6ORCID,Olivieri Anna1ORCID,Torroni Antonio1ORCID

Affiliation:

1. Dipartimento di Biologia e Biotecnologie “Lazzaro Spallanzani”, Università di Pavia , 27100 Pavia, Italy

2. Vertebrate Genome Laboratory, The Rockefeller University , New York, NY 10065, USA

3. Dipartimento di Scienze e Politiche Ambientali, Università degli Studi di Milano , 20133 Milan, Italy

4. IRCCS Istituto delle Scienze Neurologiche di Bologna, Programma di Neurogenetica , 40139 Bologna, Italy

5. Dipartimento di Chimica, Biologia e Biotecnologie, Università di Perugia , 06123 Perugia, Italy

6. Dipartimento di Bioscienze, Università degli Studi di Milano , 20133 Milan, Italy

7. Genomic and Post-Genomic Unit, IRCCS Mondino Foundation , 27100 Pavia, Italy

8. Dipartimento di Scienze Biomediche e Neuromotorie, Università di Bologna , 40139 Bologna, Italy

9. Department of Academic Education, Central Community College , Columbus, NE 68601, USA

10. State Key Laboratory of Biocontrol, School of Ecology, Sun Yat-sen University , Guangzhou 510275, China

11. Israeli Bird Ringing Center (IBRC), Israel Ornithological Center , Tel Aviv, Israel

12. Department of Zoology, University of Extremadura , 06071 Badajoz, Spain

13. Department of Wetland Ecology, Estación Biológica de Doñana CSIC , 41092 Seville, Spain

14. Department of Zoology, University of Seville , 41012 Seville, Spain

15. Department of Biological Sciences, University of South Carolina , Columbia, SC 29208, USA

16. Institute of Biological Sciences, Cardinal Stefan Wyszyński University in Warsaw , 01-938 Warsaw, Poland

17. Ecologie Systématique Evolution, Université Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay , 91405, Orsay Cedex, France

18. Department of Biological Sciences, California State Polytechnic University - Pomona , Pomona, CA 91767, USA

Abstract

Abstract The barn swallow (Hirundo rustica) poses a number of fascinating scientific questions, including the taxonomic status of postulated subspecies. Here, we obtained and assessed the sequence variation of 411 complete mitogenomes, mainly from the European H. r. rustica, but other subspecies as well. In almost every case, we observed subspecies-specific haplogroups, which we employed together with estimated radiation times to postulate a model for the geographical and temporal worldwide spread of the species. The female barn swallow carrying the Hirundo rustica ancestral mitogenome left Africa (or its vicinity) around 280 thousand years ago (kya), and her descendants expanded first into Eurasia and then, at least 51 kya, into the Americas, from where a relatively recent (<20 kya) back migration to Asia took place. The exception to the haplogroup subspecies specificity is represented by the sedentary Levantine H. r. transitiva that extensively shares haplogroup A with the migratory European H. r. rustica and, to a lesser extent, haplogroup B with the Egyptian H. r. savignii. Our data indicate that rustica and transitiva most likely derive from a sedentary Levantine population source that split at the end of the Younger Dryas (YD) (11.7 kya). Since then, however, transitiva received genetic inputs from and admixed with both the closely related rustica and the adjacent savignii. Demographic analyses confirm this species’ strong link with climate fluctuations and human activities making it an excellent indicator for monitoring and assessing the impact of current global changes on wildlife.

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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