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Conservation genetics and genetic mating system of the yellow-shouldered blackbird (Agelaius xanthomus), an endangered island endemic

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An Erratum to this article was published on 20 June 2016

Abstract

The yellow-shouldered blackbird (Agelaius xanthomus) is a managed endemic species in Puerto Rico that experienced a bottleneck in the 1970s and currently faces high levels of brood parasitism and habitat loss. Little is known about its overall genetic profile and genetic mating system, which potentially shapes effective population size by contributing to variation in reproductive success. Here I used nine microsatellite loci to characterize the population genetics and mating system of a southwestern Puerto Rican population. Although the population showed no evidence of inbreeding, it had significantly lower allelic diversity, effective population size, and expected heterozygosity than both island and continental populations of the related red-winged blackbird (A. phoeniceus). In particular, the low effective population size of the yellow-shouldered blackbird (~71, 18 % of the 2012 census size) raises concerns about its long-term viability. Paternity tests on 30 nests provided the first evidence of genetic polyandry in this species. Of all young, 23 % were extra-pair (sired by a male other than the social father), and 37 % of nests contained extra-pair young, which does not differ from proportions observed in red-winged blackbirds. Extra-pair paternity was not found to contribute significantly to variation in individual reproductive output, suggesting the bottleneck is more likely to have contributed to the current population genetic profile than the species’ mating system. Together, these data suggest that while genetic diversity on the individual level may be intact, the population as a whole remains vulnerable to adverse stochastic events and loss of evolutionary potential.

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References

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Barker FK, Vandergon AJ, Lanyon SM (2008) Species status of the Red-shouldered blackbird (Agelaius assimilis): Implications for ecological, morphological, and behavioral evolution in Agelaius. Auk 125:87–94

    Article  Google Scholar 

  • Barnés V (1945) A new form of Agelaius from Mona Island, Puerto Rico. Auk 62:299–300

    Article  Google Scholar 

  • Charlesworth B (2009) Effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10:195–205

    Article  CAS  PubMed  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crawford DJ, Ruiz E, Stuessy TF, Tepe E, Aqeveque P, Gonzalez F, Jensen RJ, Anderson GJ, Bernardello G, Baeza CM, Swenson U, Silva OM (2001) Allozyme diversity in endemic flowering plant species of the Juan Fernández Archipelago, Chile: ecological and historical factors with implications for conservation. Am J Bot 88:2195–2203

    Article  CAS  PubMed  Google Scholar 

  • Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper & Row, New York

    Google Scholar 

  • Cruz A, López-Ortiz R, Ventosa-Febles EA, Wiley JW, Nakamura TK, Ramos-Álvarez KR, Post W (2005) Ecology and management of shiny cowbirds (Molothrus bonariensis) and endangered yellow-shouldered blackbirds (Agelaius xanthomus) in Puerto Rico. Ornithol Monogr 57:38–44

    Article  Google Scholar 

  • Delrieu-Trottin E, Maynard J, Planes S (2014) Endemic and widespread coral reef fishes have similar mitochondrial genetic diversity. Proc R Soc Lond B 281:20141068

    Article  Google Scholar 

  • Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170

    Article  PubMed  PubMed Central  Google Scholar 

  • Díaz-Rodríguez A, Lewis AR (2006) Growth patterns of nestlings and other aspects of reproductive biology of Agelaius xanthomus in artificial nesting structures: final report. USFWS, Boquerón, PR, pp 56

  • Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214

    Article  CAS  PubMed  Google Scholar 

  • Elphick CS, Reed JM, Delehanty DJ (2007) Applications of reproductive biology to bird conservation and population management. In: Jamieson BGM (ed) Reproductive biology and phylogeny of birds (Aves). Science Publishers, Enfield, pp 367–399

    Google Scholar 

  • Evans BJ, Charlesworth B (2013) The effect of nonindependent mate pairing on the effective population size. Genetics 193:545–556

    Article  PubMed  PubMed Central  Google Scholar 

  • Frankham R (1995a) Effective population size/adult population size rations in wildlife: a review. Genet Res 66:95–107

    Article  Google Scholar 

  • Frankham R (1995b) Inbreeding and extinction: a threshold effect. Conserv Biol 9:792–799

    Article  Google Scholar 

  • Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327

    Article  PubMed  Google Scholar 

  • Frankham R (1998) Inbreeding and extinction: island populations. Conserv Biol 12:665–675

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics. Cambridge University Press, New York

    Book  Google Scholar 

  • Friedman NR, Hofmann CM, Kondo B, Omland KE (2009) Correlated evolution of migration and sexual dichromatism in the New World orioles (Icterus). Evolution 63:3269–3274

    Article  PubMed  Google Scholar 

  • García-Navas V, Ferrer ES, Bueno-Enciso J, Barrientos R, Sanz JJ, Ortego J (2014) Extra-pair paternity in Mediterranean blue tits: socioecological factors and the opportunity for sexual selection. Behav Ecol 25:228–238

    Article  Google Scholar 

  • Gray EM (1996) Female control of offspring paternity in a western population of red-winged blackbirds (Agelaius phoeniceus). Behav Ecol Sociobiol 38:267–278

    Article  Google Scholar 

  • Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212

    Article  CAS  PubMed  Google Scholar 

  • Haydock J, Koenig WD (2002) Reproductive skew in the polygynandrous acorn woodpecker. Proc Natl Acad Sci 99:7178–7183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holman L, Kokko H (2013) The consequences of polyandry for population viability, extinction risk and conservation. Philos Trans R Soc Lond Ser B 368:20120053

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P, Heiberger RM, Schuetzenmeister A (2014) Multcomp: simultaneous inference in general parametric. Biom J 50:346–363

    Article  Google Scholar 

  • Hundertmark KJ, Van Daele LJ (2010) Founder effect and bottleneck signatures in an introduced, insular population of elk. Conserv Genet 11:139–147

    Article  Google Scholar 

  • Johnsen A, Andersen V, Sunding C, Lifjeld JT (2000) Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296–299

    Article  CAS  PubMed  Google Scholar 

  • Johnson DL (1977) Inbreeding in populations with overlapping generations. Genetics 87:581–591

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones OR, Wang JL (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555

    Article  PubMed  Google Scholar 

  • Jorde PE, Ryman N (1995) Temporal allele frequency change and estimation of effective size in populations with overlapping generations. Genetics 139:1077–1090

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kempenaers B, Verheyren GR, Dhondt AA (1997) Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492

    Article  Google Scholar 

  • Kimura M, Ohta T (1978) Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc Natl Acad Sci USA 75:2868–2872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38

    Article  Google Scholar 

  • Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460

    Article  CAS  PubMed  Google Scholar 

  • Liu IA, Johndrow J, Abe J, Lüpold S, Yasukawa K, Westneat DF, Nowicki S (in press) Genetic diversity does not explain variation in extra-pair paternity in multiple populations of a songbird. J Evol Biol

  • López-Ortiz R, Ventosa-Febles EA, Reitsma LR, Hengstenberg D, Deluca W (2002) Increasing nest success in the yellow-shouldered blackbird Agelaius xanthomus in southwest Puerto Rico. Biol Conserv 108:259–263

    Article  Google Scholar 

  • Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Luikart G, Allendorf F, Cornuet J-M, Sherwin W (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  CAS  PubMed  Google Scholar 

  • Maki M, Yamashiro T, Matsumura S (2003) High levels of genetic diversity in island populations of the island endemic Suzukia luchuensis (Labiatae). Heredity 91:300–306

    Article  CAS  PubMed  Google Scholar 

  • Medina-Miranda R, López-Ortiz R, Ramos-Álvarez K, Cruz-Burgos J, McKenzie P, Swinnerton K, Ortega C, Cruz A, Liu I, Lacy R, Miller P, Díaz-Soltero H, Traylor-Holzer K (2013) Yellow-shouldered blackbird/shiny cowbird population and habitat viability assessment workshop final report. IUCN SSC Conservation Breeding Specialist Group, Apple Valley

    Google Scholar 

  • Nunney L (1993) The influence of mating system and overlapping generations on effective population size. Evolution 47:1329–1341

    Article  Google Scholar 

  • Odom KJ, Hall ML, Riebel K, Omland KE, Langmore NE (2014) Female song is widespread and ancestral in songbirds. Nat Commun 5:3379

    Article  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Phillipsen IC, Bowerman J, Blouin M (2010) Effective number of breeding adults in Oregon spotted frogs (Rana pretiosa): genetic estimates at two life stages. Conserv Genet 11:737–745

    Article  Google Scholar 

  • Piry S, Luikart G, Cornuet J-M (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Plesnar-Bielak A, Skrzynecka AM, Prokop ZM, Radwan J (2012) Mating system affects population performance and extinction risk under environmental challenge. Proc R Soc B 279:4661–4667

    Article  PubMed  PubMed Central  Google Scholar 

  • Post W (1981) Biology of the yellow-shouldered blackbird (Agelaius) on a tropical island. Bull Fla State Mus Biol Sci 26:123–205

    Google Scholar 

  • Post W, Wiley JW (1976) The yellow-shouldered blackbird—present and future. Am Birds 30:13–20

    Google Scholar 

  • Post W, Wiley JW (1977) Reproductive interactions of shiny cowbird and yellow-shouldered blackbird. Condor 79:176–184

    Article  Google Scholar 

  • Price JJ (2009) Evolution and life-history correlates of female song in the New World blackbirds. Behav Ecol 20:967–977

    Article  Google Scholar 

  • Price JJ, Lanyon SM, Omland KE (2009) Losses of female song with changes from tropical to temperate breeding in the New World blackbirds. Proc R Soc Lond Ser B 276:1971–1980

    Article  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    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 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Saether BE, Engen S, Lande R, Møller AP, Bensch S, Hasselquist D, Beier J, Leisler B (2004) Time to extinction in relation to mating system and type of density regulation in populations with two sexes. J Anim Ecol 73:925–934

    Article  Google Scholar 

  • Sardell RJ, Arcese P, Keller LF, Reid JM (2012) Are there indirect fitness benefits of female extra-pair reproduction? Lifetime reproductive success of within-pair and extra-pair offspring. Am Nat 179:779–793

    Article  PubMed  Google Scholar 

  • Schlicht E, Kempenaers B (2013) Effects of social and extra-pair mating on sexual selection in blue tits (Cyanistes caeruleus). Evolution 67:1420–1434

    PubMed  Google Scholar 

  • Searcy WA, Yasukawa K (1995) Polygyny and sexual selection in red-winged blackbirds. Princeton University Press, Princeton

    Book  Google Scholar 

  • Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629

    Article  PubMed  Google Scholar 

  • Soulé M (1980) Thresholds for survival: maintaining fitness and evolutionary potential. In: Apollonio M, Festa-Bianchet M, Soulé M, Wilcox B (eds) Conservation biology: an evolutionary-ecological perspective. Sinauer, Sunderland, MD, pp 151–169

    Google Scholar 

  • Stephens PA, Sutherland WJ (2000) Vertebrate mating systems, Allee effects and conservation. In: Apollonio M, Festa-Bianchet M, Mainardi D (eds) Vertebrate mating systems. World Scientific Publishing, London, pp 186–213

    Chapter  Google Scholar 

  • Sugg DW, Chesser RK (1994) Effective population sizes with multiple paternity. Genetics 137:1147–1155

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tallmon DA, Koyuk A, Luikart G, Beaumont MA (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Resour 8:299–301

    Article  PubMed  Google Scholar 

  • Traill LW, Bradshaw CJA, Brook BW (2007) Minimum viable population size: a meta-analysis of 30 years of published estimates. Biol Conserv 139:159–166

    Article  Google Scholar 

  • Tsuji K, Tsuji N (1998) Indices of reproductive skew depend on average reproductive success. Evol Ecol 12:141–152

    Article  CAS  Google Scholar 

  • USFWS (1976) Determination of endangered status for yellow-shouldered blackbird and determination of critical habitat. Federal Register, pp 51019–51022

  • USFWS (1996) Yellow-shouldered blackbird (Agelaius xanthomus) revised recovery plan. Fish and Wildlife Service, Atlanta, GA, p 77

    Google Scholar 

  • USFWS (2011) Mariquita or yellow-shouldered blackbird (Agelaius xanthomus) 5-Year Review: summary and evaluation. Fish and Wildlife Service, Boquerón, PR, p 34

    Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Wang JL (2009) A new method for estimating effective population sizes from a single sample of multilocus genotypes. Mol Ecol 18:2148–2164

    Article  PubMed  Google Scholar 

  • Waples RS (2010) Spatial-temporal stratifications in natural populations and how they affect understanding and estimation of effective population size. Mol Ecol Resour 10:785–796

    Article  PubMed  Google Scholar 

  • Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756

    Article  PubMed  Google Scholar 

  • Watterson GA (1984) Allele frequencies after a bottleneck. Theor Popul Biol 26:387–407

    Article  Google Scholar 

  • Webster MS, Pruett-Jones S, Westneat DF, Arnold SJ (1995) Measuring the effects of pairing success, extra-pair copulations and mate quality on the opportunity for sexual selection. Evolution 49:1147–1157

    Article  Google Scholar 

  • Westneat DF (1993) Polygyny and extrapair fertilizations in eastern red-winged blackbirds (Agelaius phoeniceus). Behav Ecol 4:49–60

    Article  Google Scholar 

  • Westneat DF, Mays HL (2005) Tests of spatial and temporal factors influencing extra-pair paternity in red-winged blackbirds. Mol Ecol 14:2155–2167

    Article  CAS  PubMed  Google Scholar 

  • Wetzel DP, Westneat DF (2009) Heterozygosity and extra-pair paternity: biased tests result from the use of shared markers. Mol Ecol 18:2010–2021

    Article  PubMed  Google Scholar 

  • Wiley JW, Post W, Cruz A (1991) Conservation of the yellow-shouldered blackbird Agelaius xanthomus, an endangered West Indian species. Biol Conserv 55:119–138

    Article  Google Scholar 

  • Wright S (1938) Size of population and breeding structure in relation to evolution. Science 87:430–431

    Google Scholar 

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Acknowledgments

I thank Steve Nowicki for advice and guidance, Mohamed Noor for use of lab space, and Matt Johnson, Suzanne McGaugh, and two anonymous reviewers for comments on previous versions of the manuscript. For access to field sites, I am extremely grateful to the Puerto Rico Department of Natural and Environmental Resources, especially Roseanne Medina-Miranda, Ricardo López-Ortiz, and Katsí Ramos-Álvarez, and to the U.S. Fish and Wildlife Service, especially José Cruz-Burgos, Cameron Shaw, and the staff at Cabo Rojo National Wildlife Refuge. Field protocols were approved by Duke University’s Institutional Animal Care and Use Committee and all relevant local, national and international institutions. This work was funded by a National Science Foundation (NSF) Graduate Research Fellowship, an NSF Dissertation Improvement Grant (award no. IOS-1110782), a Sigma Delta Epsilon Fellowship from Graduate Women in Science, and the Office of the Provost at Duke University.

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Liu, I.A. Conservation genetics and genetic mating system of the yellow-shouldered blackbird (Agelaius xanthomus), an endangered island endemic. Conserv Genet 16, 1041–1053 (2015). https://doi.org/10.1007/s10592-015-0721-5

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