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Genetic evidence of hybridization between Magellanic (Sphensicus magellanicus) and Humboldt (Spheniscus humboldti) penguins in the wild

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Abstract

The process of hybridization between closely related species plays an important role in defining the genetic integrity and overall genetic diversity of species. The distribution range of Magellanic (Spheniscus magellanicus) and Humboldt (Spheniscus humboldti) penguins is predominantly allopatric; however, the species share a region of sympatry where they may hybridize. We analyzed four types of genetic markers (including nuclear and mitochondrial markers) to assess their utility in detecting hybridization events between Magellanic and Humboldt penguins. Genetic assessment of non-introgressed reference samples allowed us to identify three types of informative markers (microsatellites, major histocompatibility complex, and mitochondrial DNA) and detect positive evidence of introgressive hybridization in the wild. Four out of six putative hybrids showed positive evidence of hybridization, revealed by the detection of Humboldt mitochondrial DNA and Magellanic species-specific alleles from nuclear markers. Bayesian Structure analysis, including samples from the sympatric region of the species in the southern Pacific Ocean, confirmed the use of nuclear markers for detecting hybridization and genetic admixture of putative hybrids, but revealed relatively low levels of genetic introgression at the population level. These findings provide insights into the role of hybridization in regions of species sympatry and its potential consequences on the levels of genetic introgression, genetic diversity, and conservation of these penguin species.

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References

  • Akst EP, Boersma PD, Fleischer RC (2002) A comparison of genetic diversity between the Galápagos Penguin and the Magellanic Penguin. Conserv Genet 3:375–383

    CAS  Google Scholar 

  • Aliabadian M, Nijman V (2007) Avian hybrids: incidence and geographic distribution of hybridisation in birds. Contrib Zool 76:59–61

    Google Scholar 

  • Anderson E (1949) Introgressive hybridization. John Wiley and Sons, New York

    Google Scholar 

  • Arauco-Shapiro G, Schumacher KI, Boersma D, Bouzat JL (2020) The role of demographic history and selection in shaping genetic diversity of the Galápagos penguin (Spheniscus mendiculus). PLoS One 15(1):e0226439

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arnold ML (1992) Natural hybridization as an evolutionary process. Annu Rev Ecol Syst 23:237–261

    Google Scholar 

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Arnold ML, Buckner CM, Robinson JJ (1991) Pollen-mediated introgression and hybrid speciation in Louisiana irises. Proc Natl Acad Sci USA 88:1398–1402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baker AJ, Pereira SL, Haddrath OP, Edge KA (2006) Multiple gene evidence for expansion of extant penguins out of Antarctica due to global cooling. Proc R Soc B 273:11–17

    PubMed  Google Scholar 

  • Barton NH (2008) The effect of a barrier to gene flow on patterns of geographic variation. Genet Res (Camb) 90:139–149

    CAS  Google Scholar 

  • Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148

    Google Scholar 

  • Bertelli S, Giannini NP (2005) A phylogeny of extant penguins (Aves: Sphenisciformes) combining morphology and mitochondrial sequences. Cladistics 21:209–239

    Google Scholar 

  • BirdLife International (2018a) Spheniscus magellanicus. The IUCN Red List of Threatened Species 2018: e.T22697822A132605485. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22697822A132605485.en

  • BirdLife International (2018b) Spheniscus humboldti. The IUCN Red List of Threatened Species 2018: e.T22697817A132605004. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22697817A132605004.en

  • Boersma PD, Frere E, Kane O, Pozzi LM, Putz K, Rey AR, Rebstock GA, Simeone A, Smith J, Van Buren A, Yorio P, García Borboroglu P (2013) Magellanic penguin. In: García Borboroglu P, Boersma PD (eds) Penguins: natural history and conservation. University of Washington Press, Seattle, pp 233–263

    Google Scholar 

  • Bouzat JL, Walker BG, Boersma PD (2009) Regional genetic structure in the Magellanic penguin (Spheniscus magellanicus) suggests metapopulation dynamics. Auk 126:326–334

    Google Scholar 

  • Bouzat JL, Lyons, AC, Knafler GJ, Boersma PD (2013) Environmental determinants of genetic structure in Magellanic Penguin breeding colonies of the Atlantic and Pacific Oceans. VIII International Penguin Conference. September 2–6, 2013. Bristol, United Kingdom

  • Bullini L (1994) Origin and evolution of animal hybrid species. Trends Ecol Evol 9:422–426

    CAS  PubMed  Google Scholar 

  • Cole TL, Ksepka DT, Mitchell KJ, Tennyson AJD, Thomas DB, Pan H, Zhang G, Rawlence NJ, Wood JR, Bover P, Bouzat JL, Cooper A, Fiddaman SR, Hart T, Miller G, Ryan PG, Shepherd LD, Wilmshurst JM, Waters JM (2019) Mitogenomes uncover extinct penguin taxa and reveal island formation as a key driver of speciation. Mol Biol Evol 36:784–797

    CAS  PubMed  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland

    Google Scholar 

  • Dantas GPM, Oliveira LR, Santos AM, Flores MD, de Melo DR, Simeone A, González-Acuña D, Luna-Jorquera G, Le Bohec C, Valdés-Velásquez A, Cardeña M, Morgante JS, Vianna JA (2019) Uncovering population structure in the Humboldt penguin (Spheniscus humboldti) along the Pacific coast at South America. PLoS One 14(5):e021593

    Google Scholar 

  • DeMarais BD, Dowling TE, Douglas ME, Minckley WL, Marsh PC (1992) Origin of Gila seminuda (Teleostei: Cyprinidae) through introgressive hybridization: implications for evolution and conservation. Proc Natl Acad Sci USA 89:2747–2751

    CAS  PubMed  PubMed Central  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Google Scholar 

  • Endler JA (1977) Natural selection in the wild. Princeton University Press, Princeton

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    CAS  PubMed  Google Scholar 

  • García Borboroglu P, Boersma PD (eds) (2013) Penguins: natural history and conservation. University of Washington Press, Seattle

    Google Scholar 

  • Gavryushkina A, Heath TA, Ksepka DT, Stadler T, Welch D, Drummond AJ (2017) Bayesian total-evidence dating reveals the recent crown radiation of penguins. Syst Biol 66:57–73

    PubMed  Google Scholar 

  • Gholanhosseini A, Vardakis M, Aliabadian M, Nijman V, Vonk R (2013) Hybridization between sister taxa versus non-sister taxa: a case study in birds. Bird Study 60:195–201

    Google Scholar 

  • Gownaris NJ, Boersma PD (2019) Sex-biased survival contributes to population decline in a long-lived seabird, the Magellanic Penguin. Ecol Appl 29(1):e01826

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gownaris NJ, García Borboroglu P, Boersma PD (2020) Sex ratio is variable and increasingly male biased at two colonies of Magellanic penguins. Ecology 101(3):e02939

    PubMed  Google Scholar 

  • Grant PR, Grant BR (1992) Hybridization of bird species. Science 256:193–197

    CAS  PubMed  Google Scholar 

  • Grant SW, Duffy DC, Leslie RW (1994) Allozyme phylogeny of Spheniscus penguins. Auk 111:716–720

    Google Scholar 

  • Griffiths R, Double MC, Orr K, Dawson JG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075

    CAS  PubMed  Google Scholar 

  • Griffiths R, Tiwari B (1995) Sex of the last wild Spix’s macaw. Nature 375:454

    CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harrison RG (1990) Hybrid zones: windows on the evolutionary process. Oxf Surv Evol Biol 7:69–128

    Google Scholar 

  • Harrison RG (1993) Hybrid zones and the evolutionary process. Oxford University Press, Oxford

    Google Scholar 

  • Harrison RG, Larson EL (2014) Hybridization, introgression, and the nature of species boundaries. J Hered 105(Suppl. 1):795–809

    PubMed  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321

    CAS  Google Scholar 

  • Hebert PDN, Ratnasingham S, de Waard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B 270(Suppl. 1):S96–S99

    CAS  Google Scholar 

  • Hubbs CL (1955) Hybridization between fish species in nature. Syst Zool 4:1–20

    Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    CAS  PubMed  Google Scholar 

  • Jančúchová-Lásková J, Landová E, Frynta D (2015) Are genetically distinct lizard species able to hybridize? A review. Curr Zool 61:155–180

    Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic, an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    PubMed  PubMed Central  Google Scholar 

  • Kikkawa EF, Tsuda TT, Naruse TK, Sumiyama D, Fukuda M, Kurita M, Murata K, Wilson RP, Lemaho Y, Tsuda M, Kulski JK, Inoko H (2005) Analysis of the sequence variations in the Mhc DRB1-like gene of the endangered Humboldt penguin (Spheniscus humboldti). Immunogenetics 57:99–107

    CAS  PubMed  Google Scholar 

  • Kikkawa EF, Tsuda TT, Naruse TK, Sumiyama D, Fukuda M, Kurita M, Wilson RP, Lemaho Y, Miller GD, Tsuda M, Murata K, Kulski JK, Inoko H (2009) Trans-species polymorphism of the Mhc DRB1-like gene in banded penguins (genus Spheniscus). Immunogenetics 61:341–352

    CAS  PubMed  Google Scholar 

  • Knaffler GJ, Clark JA, Boersma PD, Bouzat JL (2012) MHC diversity and mate choice in the Magellanic Penguin, Spheniscus magellanicus. J Hered 103:759–768

    Google Scholar 

  • Kraus F, Miyamoto MM (1990) Mitochondrial genotype of a unisexual salamander of hybrid origin is unrelated to either of its nuclear haplotypes. Proc Natl Acad Sci USA 87:2235–2238

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ksepka DT, Bertelli S, Giannini NP (2006) The phylogeny of the living and fossil Sphenisciformes (penguins). Cladistics 22:412–441

    Google Scholar 

  • Mallet J (2005) Hybridization as an invasion of the Genome. Trends Ecol Evol 20:229–237

    PubMed  Google Scholar 

  • Mallet J (2007) Hybrid speciation. Nature 446:279–283

    CAS  PubMed  Google Scholar 

  • McCarthy EM (2006) Handbook of Avian hybrids. Oxford University Press, Oxford

    Google Scholar 

  • Morgan-Richards M, Smissen RD, Shepard LD, Wallis GP, Hayward JJ, Chan CH, Chambers GK, Chapman HM (2009) A review of genetic analyses of hybridisation in New Zealand. J R Soc NZ 39:15–34

    Google Scholar 

  • Morrison KW, Sagar PM (2014) First record of interbreeding between a Snares crested (Eudyptes robustus) and erect-crested penguin (E. sclateri). Notornis 61:109–112

    Google Scholar 

  • Napier R (1968) Erect-crested and Rockhopper Penguins interbreeding in the Falkland Islands. Br Antarct Surv Bull 16:71–72

    Google Scholar 

  • Nielsen EE, Hansen MM, Ruzzante DE, Meldrup D, Gronkjaer P (2003) Evidence of a hybrid-zone in Atlantic cod (Gadus morhua) in the Baltic and Danish Belt Sea revealed by individual admixture analysis. Mol Ecol 12:1497–1508

    PubMed  Google Scholar 

  • Ottenburghs J, Ydenberg RC, Van Hooft P, Van Wieren SE, Prins HHT (2015) The Avian Hybrids Project: gathering the scientific literature on avian hybridization. Ibis 157:892–894

    Google Scholar 

  • Price T (2008) Speciation in birds. Roberts and Company Publishers, Greenwood Village

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Randler C (2002) Avian hybridization, mixed pairing and female choice. Anim Behav 63:103–119

    Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    PubMed  Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

    Google Scholar 

  • Rieseberg LH, van Fossen C, Desrochers A (1995) Hybrid speciation accompanied by genomic reorganization in wild sunflowers. Nature 375:313–316

    CAS  Google Scholar 

  • Sambrook J, Fritschi EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Schlosser JA, Dubach JM, Garner TWJ, Araya B, Bernal M, Simeone A, Smith KA, Wallace RS (2009) Evidence for gene flow differs from observed dispersal patterns in the Humboldt penguin, Spheniscus humboldti. Conserv Genet 10:839–849

    CAS  Google Scholar 

  • Schwarz D, Matta BM, Shakir-Botteri NL, McPheron BA (2005) Host shift to an invasive plant triggers rapid animal hybrid speciation. Nature 436:546–549

    CAS  PubMed  Google Scholar 

  • Schwenk K, Brede N, Striet B (2008) Introduction. Extent, processes and evolutionary impact of interspecific hybridization in animals. Phil Trans R Soc B 363:2805–2811

    PubMed  PubMed Central  Google Scholar 

  • Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analysis. Can J Zool 69:82–90

    CAS  Google Scholar 

  • Sibley CG, Ahlquist JE (1990) Phylogeny and classification of the birds: a study in molecular evolution. Yale University Press, New Haven

    Google Scholar 

  • Simeone A, Hiriart-Bertrand L, Reyes-Arriagada R, Halpern M, Dubach J, Wallace R, Pütz K, Lüthi B (2009) Heterospecific pairing and hybridization between wild humboldt and magellanic penguins in Southern Chile. The Condor 111:544–550

    Google Scholar 

  • Simpson KNG (1985) A Rockhopper x royal penguin hybrid from Macquarie Island. Aust Bird Watch 11:35–45

    Google Scholar 

  • Slack KE, Jones CM, Ando T, Harrison GL, Fordyce RE, Arnason U, Penny D (2006) Early penguin fossils, plus mitochondrial genomes, calibrate avian evolution. Mol Biol Evol 23:1144–1155

    CAS  PubMed  Google Scholar 

  • Slotte T, Huang H, Lascoux M, Ceplitis A (2008) Polyploid speciation did not confer instant reproductive isolation in Capsella (Brassicaceae). Mol Biol Evol 25:1472–1481

    CAS  PubMed  Google Scholar 

  • Subramanian S, Beans-Picón G, Swaminathan SK, Millar CD, Lambert DM (2013) Evidence for a recent origin of penguins. Biol Lett 9:20130748

    PubMed  PubMed Central  Google Scholar 

  • Thumser NN, Karron JD (1994) Patterns of genetic polymorphism in five species of penguins. Auk 111:1018–1022

    Google Scholar 

  • Thumser NN, Karron JD, Ficken MS (1996) Interspecific variation in the calls of Spheniscus penguins. Wilson Bull 108:72–79

    Google Scholar 

  • Twyford AD, Ennos RA (2012) Next-Generation hybridization and introgression. Heredity 108:179–189

    CAS  PubMed  Google Scholar 

  • Vences M, Wake DB (2007) Speciation, species boundaries and phylogeography of amphibians. In: Heatwole H, Tyler MJ (eds) Amphibian biology systematics, 7th edn. Surrey Beatty & Sons Pty Limited, Chipping Norton, pp 2613–2671

    Google Scholar 

  • Vianna JA, Cortes M, Ramos B, Sallaberry-Pincheira N, González-Acuña D, Dantas GPM, Morgante J, Simeone A, Luna-Jorquera G (2014) Changes in abundance and distribution of Humboldt penguin Spheniscus humboldti. Mar Ornithol 42:153–159

    Google Scholar 

  • Vianna JA, Fernandes FAN, Frugone MJ, Figueiró HV, Pertierra LR, Noll D, Bi K, Wang-Claypool CY, Lowther A, Parker P, Le Bohec C, Bonadonna F, Wienecke B, Pistorius P, Steinfurth A, Burridge CP, Dantas GPM, Poulin E, Simison WB, Henderson J, Eizirik E, Nery MF, Bowie RCK (2020) Genome-wide analyses reveal drivers of penguin diversification. Proc Natl Acad Sci USA 117(36):22303–22310

    CAS  PubMed  PubMed Central  Google Scholar 

  • White RW, Clausen AP (2002) Rockhopper Eudyptes chrysocome x Macaroni E. chrysolophus penguin hybrids apparently breeding in the Falkland Islands. Mar Ornithol 30:40–42

    Google Scholar 

  • Woehler EJ, Gilbert CA (1990) Hybrid Rockhopper-Macaroni Penguins, Interbreeding and Mixed Species Pairs at Heard and Marion Islands. Emu 90:198–201

    Google Scholar 

  • Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15:1039–1053

    Google Scholar 

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Acknowledgements

We would like to thank Javier Simonetti for helping in the processing of collection permits from Chile, and Manuel R. Paredes Oyarzún and Hernán Rivera Meléndez (CONAF, Chile) for helping with CONAF permits and logistic support during collection of samples at Chiloé. We are also thankful to Ariel Valle for his help during field collections at the Ahuenco colony. Tim Snyder, Curator of Birds at the Chicago Zoological Society’s Brookfield Zoo, coordinated the sampling and transferring of Humboldt penguin samples from the Brookfield Zoo to be used as the Humboldt reference population. This study was part of Eric Hibbets’ thesis submitted to Bowling Green State University in partial fulfillment of the requirements for the degree of Master of Science.

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  1. Department of Biological Sciences, Bowling Green State University, Bowling Green, OH, 43403, USA

    Eric M. Hibbets, Katelyn I. Schumacher, Hannah B. Scheppler & Juan L. Bouzat

  2. Department of Biology, Center for Ecosystem Sentinels, University of Washington, Seattle, WA, 98195, USA

    P. Dee Boersma

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  1. Eric M. Hibbets
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Hibbets, E.M., Schumacher, K.I., Scheppler, H.B. et al. Genetic evidence of hybridization between Magellanic (Sphensicus magellanicus) and Humboldt (Spheniscus humboldti) penguins in the wild. Genetica 148, 215–228 (2020). https://doi.org/10.1007/s10709-020-00106-2

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