Invasion genetics: Lessons from a ubiquitous bird, the house sparrow passer domesticus

Current Zoology

Volumn 61, Issue 3, 2015, Pages 465-476

  Liebl, Andrea L ^a   Schrey, Aaron W ^b   Andrew, Samuel C ^c   Sheldon, Elizabeth L ^c   Griffith, Simon C ^c  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b Armstrong State University   (United States)

^c MACQUARIE UNIVERSITY   (Australia)

Author keywords

House sparrow; Invasive; Passer domesticus

Indexed keywords

AVES; PASSER DOMESTICUS; VERTEBRATA;

EID: 84929260840     PISSN: 16745507     EISSN: None     Source Type: Journal    
DOI: 10.1093/czoolo/61.3.465     Document Type: Article

References (115)

1. Agrawal AA, 2001. Phenotypic plasticity in the interactions and evolution of species. Science 294: 321–326.
2. Altwegg R, Ringsby TH, Sæther BE, 2000. Phenotypic correlates and consequences of dispersal in a metapopulation of house sparrows Passer domesticus. Journal of Animal Ecology 69: 762–770.
3. Anderson TR, 2006. Biology of the ubiquitous house sparrow: From genes to populations. New York: Oxford University Press.
4. Baalsrud HT, Sæther BE, Hagen IJ, Myhre AM, Ringsby TH et al., 2014. Effects of population characteristics and structure on estimates of effective population size in a house sparrow metapopulation. Molecular Ecolology 23: 2653–2668.
5. Bakker JD, Wilson SD, 2004. Using ecological restoration to constrain biological invasion. Journal of Applied Ecology 41: 1058–1064.
6. Bates JM, Zink RM, 1992. Seasonal variation in gene frequencies in the house sparrow Passer domesticus. The Auk. 109: 658– 662.
7. Bjordal H, Cole S, Parkin D, 1986. Genetic differentiation among some populations of the house sparrow Passer domesticus from southwestern Norway. Hereditas 105: 107–114.
8. Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP et al., 2011. A proposed unified framework for biological invasions. Trends in Ecology & Evolution 26: 333–339.
9. Bókony V, Kulcsár A, Liker A, 2009. Does urbanization select for weak competitors in house sparrows. Oikos 119: 437–444.
10. Bókony V, Kulcsár A, Tóth Z, Liker A, 2012. Personality Traits and behavioral syndromes in differently urbanized populations of house sparrows Passer domesticus. PLoS ONE 7: e36639.
11. Bókony V, Lendvai ÁZ, Vágási CI, Pătraş L, Pap PL et al., 2014. Necessity or capacity? Physiological state predicts problemsolving performance in house sparrows. Behavioral Ecology 25: 124–135.
12. Borer ET, Harpole WS, Adler PB, Lind EM, Orrock JL et al., 2014. Finding generality in ecology: A model for globally distributed experiments. Methods in Ecology and Evolution 5: 65–73.
13. Bossdorf O, Arcuri D, Richards CL, Pigliucci M, 2010. Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana. Evolutionary Ecology 24: 541–553.
14. Brommer JE, Hanski IK, Kekkonen J, Väisänen RA, 2014. Size differentiation in Finnish house sparrows follows Bergmann's rule with evidence of local adaptation. Journal of Evolutionary Biology 27: 737–747.
15. Burke T, Bruford M, 1987. DNA fingerprinting in birds. Nature 327: 149–152.
16. Cassey P, Blackburn TM, Russell GJ, Jones KE, Lockwood JL, 2004. Influences on the transport and establishment of exotic bird species: An analysis of the parrots (Psittaciformes) of the world. Global Change Biology 10: 417–426.
17. Clegg SM, Degnan SM, Kikkawa J, 2002. Genetic consequences of sequential founder events by an island-colonizing bird. Proceedings of the National Academy of Sciences 99: 8127– 8132.
18. Cole SR, Parkin DT, 1981. Enzyme polymorphisms in the house sparrow Passer domesticus. Biological Journal of the Linnean Society 15: 13–22.
19. Cordero PJ, Wetton JH, Parkin DT, 1999. Extra-pair paternity and male badge size in the house sparrow. Journal of Avian Biology 30: 97–102.
20. Davidson AM, Jennions M, Nicotra AB, 2011. Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecology Letters 14: 419– 431.
21. Dawson DA, Burke T, Hansson B, Pandhal J, Hale MC et al., 2006. A predicted microsatellite map of the passerine genome based on chicken-passerine sequence similarity. Molecular Ecology 15: 1299–1320.
22. Dawson DA, Horsburgh GJ, Küpper C, Stewart IRK, Ball AD et al., 2010. New methods to identify conserved microsatellite loci and develop primer sets of high cross-species utility: As demonstrated for birds. Molecular ecology resources 10: 475– 494.
23. Dawson DA, Horsburgh GJ, Krupa AP, Stewart IRK, Skjelseth S et al., 2012. Microsatellite resources for Passeridae species: A predicted microsatellite map of the house sparrow Passer domesticus. Molecular ecology resources 12: 501–523.
24. Dlugosch KM, Parker IM, 2008. Founding events in species invasions: Genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology 17: 431–449.
25. Duckworth RA, Badyaev AV, 2007. Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proceedings of the National Acadamy of Science 104: 15017–15022.
26. Edly-Wright C, Schwagmeyer P, Parker PG, Mock DW, 2007. Genetic similarity of mates, offspring health and extrapair fer tilization in house sparrows. Animal behaviour 73: 367–378.
27. Engen S, Ringsby TH, Saether BE, Lande R, Jensen H et al., 2007. Effective size of fluctuating populations with two sexes and overlapping generations. Evolution 61: 1873–1885.
28. Fleischer RC, Johnston RF, 1982. Natural selection on body size and proportions in house sparrows. Nature 298: 747–749.
29. Fleischer RC, 1983. A comparison of theoretical and electrophoretic assessments of genetic structure in populations of the house sparrow Passer domesticus. Evolution 37: 1001–1009.
30. Fleischer RC, Johnston RF, Klitz WJ, 1983. Allozymic heterozygosity and morphological variation in house sparrows. Nature 304: 628–630.
31. Fleischer RC, Lowther PE, Johnston RF, 1984. Natal dispersal in house sparrows: Possible causes and consequences. Journal of Field Ornithology 55: 444–456.
32. Garnier S, Durand P, Arnathau C, Risterucci AM, Esparza-Salas R et al., 2009. New polymorphic microsatellite loci in the house sparrow Passer domesticus. Molecular Ecology Resources 9: 1063–1065.
33. Gaston KJ, 2010. Valuing common species. Science 327: 154– 155.
34. Gavett AP, Wakeley JS, 1986a. Blood constituents and their relation to diet in urban and rural house sparrows. Condor 88: 279–284.
35. Griffith SC, Owens IPF, Burke T, 1999a. Female choice and annual reproductive success favour less-ornamented male house sparrows. Proceedings of the Royal Society, B. 266.
36. Griffith SC, Stewart IRK, Dawson DA, Owens IPF, Burke T, 1999b. Contrasting levels of extral pair paternity in mainland and island populations of the house sparrow Passer domesticus: Is there an 'island effect'? Biological Journal of the Linnean Society 68: 303–316.
37. Griffith SC, Dawson DA, Jensen H, Ockendon N, Greig C et al., 2007. Fourteen polymorphic microsatellite loci characterized in the house sparrow Passer domesticus (Passeridae, Aves). Molecular Ecology Notes 7: 333–336.
38. Grinnell J, 1919. The English sparrow has arrived in death valley: An experiment in nature. American naturalist 53: 468–472.
39. Hagen IJ, Billing AM, Rønning B, Pedersen SA, Pärn H et al., 2013. The easy road to genome-wide medium density SNP screening in a non-model species: Development and application of a 10 K SNP-chip for the house sparrow Passer domesticus. Molecular Ecology Resources 13: 429–439.
40. Higgins P, Peter J, 2002. Handbook of Australian, New Zealand and Antarctic Birds. Vol. 6: Pardalotes to Shrike-thrushes. Victoria: Oxford University Press.
41. Hole DG, Whittingham MJ, Bradbury RB, Anderson GQA, Lee PLM et al., 2002a. Widespread local house-sparrow extinctions. Nature 418: 931–932.
42. Holt RD, 2003. On the evolutionary ecology of species' ranges. Evolutionary Ecology Research 5: 159–178.
43. Jensen H, Bremset EM, Ringsby TH, Saether BE, 2007. Multilocus heterozygosity and inbreeding depression in an insular house sparrow metapopulation. Molecular Ecology 16: 4066– 4078.
44. Jensen H, Moe R, Hagen IJ, Holand AM, Kekkonen J et al., 2013. Genetic variation and structure of house sparrow populations: Is there an island effect? Molecular Ecology 22: 1792–1805.
45. Johnston RF, Selander RK, 1964. House sparrows: Rapid evolution of races in North America. Science 144: 548–550.
46. Johnston RF, Selander RK, 1971. Evolution in the house sparrow. II. Adaptive differentiation in North American populations. Evolution 25: 1–28.
47. Johnston RF, Selander RK, 1973. Evolution in the house sparrow. III. Variation in size and sexual dimorphism in Europe and North and South America. American Naturalist 107: 373–390.
48. Kekkonen J, Hanski IK, Jensen H, Väisänen RA, Brommer JE, 2011a. Increased genetic differentiation in house sparrows after a strong population decline: From panmixia towards structure in a common bird. Biological Conservation 144: 2931– 2940.
49. Kekkonen J, Seppä P, Hanski IK, Jensen H, Väisänen RA et al., 2011b. Low genetic differentiation in a sedentary bird: House sparrow population genetics in a contiguous landscape. Heredity 106: 183–190.
50. Kekkonen J, Jensen H, Brommer JE, 2012. Morphometric differentiation across house sparrow Passer domesticus populations in Finland in comparison with the neutral expectation for divergence. Ibis 154: 846–857.
51. Klitz W, 1973. Empirical population genetics of the North American house sparrow. Ornithological Monographs 14: 34–38.
52. Kolbe JJ, Glor RE, Rodriguez Schettino L, Lara AC, Larson A et al., 2004. Genetic variation increases during biological invasion by a Cuban lizard. Nature. 431: 177–181.
53. Koren L, Nakagawa S, Burke T, Soma KK, Wynne-Edwards KE et al., 2012. Non-breeding feather concentrations of testosterone, corticosterone and cortisol are associated with subsequent survival in wild house sparrows. Proceedings of the Royal Society B: Biological Sciences 279: 1560–1566.
54. Lack D, 1940. Variation in the introduced English sparrow. Condor 42: 239–241.
55. Lattin CR, Romero LM, 2014. Chronic stress alters concentrations of corticosterone receptors in a tissue-specific manner in wild house sparrows Passer domesticus. The Journal of Experimental Biology 217: 2601–2608.
56. Lendvai ÁZ, Chastel O, 2010. Natural variation in stress response is related to post-stress parental effort in male house sparrows. Hormones and Behavior 58: 936–942.
57. Lendvai ÁZ, Bókony V, Chastel O, 2011. Coping with novelty and stress in free-living house sparrows. Journal of Experimental Biology 214: 821–828.
58. Lever C, 2005. Naturalised Birds of the World. London: T & A D Poyser.
59. Levine JM, D'Antonio CM, 2003. Forecasting biological invasions with increasing international trade. Conservation Biology 17: 322–326.
60. Liebl AL, Martin LB, 2012. Exploratory behaviour and stressor hyper-responsiveness facilitate range expansion of an introduced songbird. Proceedings of the Royal Society B: Biological Sciences 279: 4375–4381.
61. Liebl AL, Martin LB, 2013. Stress hormone receptors change as range expansion progresses in house sparrows. Biology Letters 9: 20130181.
62. Liebl AL, Schrey AW, Richards CL, Martin LB, 2013a. Patterns of DNA methylation throughout a range expansion of an introduced songbird. Integrative and Comparative Biology 53: 351–358.
63. Liebl AL, Shimizu T, Martin LB, 2013b. Covariation among glucocorticoid regulatory elements varies seasonally in house sparrows. General and Comparative Endocrinology 183: 32– 37.
64. Liebl AL, Martin LB, 2014. Living on the edge: Range edge birds consume novel foods sooner than established ones. Behavioral Ecology 25: 1089–1096.
65. Liker A, Papp Z, Bokony V, Lendvai AZ, 2008. Lean birds in the city: Body size and condition of house sparrows along the urbanization gradient. Journal of Animal Ecology 77: 789–795.
66. Liker a, Bókony V, Kulcsár A, Tóth Z, Szabó K et al., 2009. Genetic relatedness in wintering groups of house sparrows Passer domesticus. Molecular Ecology 18: 4696–4706.
67. Lima MR, Macedo RHF, Martins TLF, Schrey AW, Martin LB et al., 2012. Genetic and morphometric divergence of an invasive bird: The introduced house sparrow Passer domesticus in Brazil. PLoS ONE 7: e53332.
68. Loiseau C, Richard M, Garnier S, Chastel O, Julliard R et al., 2009. Diversifying selection on MHC class I in the house sparrow Passer domesticus. Molecular Ecology 18: 1331– 1340.
69. Long JL, 1981. Introduced Birds of the World. New York: Universe Books.
70. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M et al., 2000. Biotic invasions: Causes, epidemiology, global consequences, and control. Ecological Applications 10: 689–710.
71. Manwell C, Baker CMA, 1975. Molecular genetics of avian proteins XIII. Protein polymorphism in three species of Australian passerines. Australian Journal of biological Sciences 28: 545– 557.
72. Martin LB, Fitzgerald L, 2005. A taste for novelty in invading house sparrows Passer domesticus. Behavioral Ecology 16: 702–707.
73. Martin LB, Alam JL, Imboma T, Liebl AL, 2010. Variation in inflammation as a correlate of range expansion in Kenyan house sparrows. Oecologia 164: 339–347.
74. Martin LB, Coon CAC, Liebl AL, Schrey AW, 2014. Surveillance for microbes and range expansion in house sparrows. Proceedings of the Royal Society B: Biological Sciences. 281: 20132690.
75. Martin LB, Liebl AL, 2014. Physiological flexibility in an avian range expansion. General and Comparative Endocrinology 206: 227–234.
76. Martin LB, Liebl AL, Kilvitis H, in press. Stresss-immune interactions in a range expanding bird. General and Comparative Endocrinology.
77. Nakagawa S, Ockendon N, Gillespie DOS, Hatchwell BJ, Burke T, 2007. Assessing the function of house sparrows’ bib size using a flexible meta-analysis method. Behavioral Ecology 18: 831– 840.
78. Neumann K, Wetton JH, 1996. Highly polymorphic microsatellites in the house sparrow Passer domesticus. Molecular Ecology 5: 307–309.
79. Ockendon N, Griffith SC, Burke T, 2009. Extrapair paternity in an insular population of house sparrows after the experimental introduction of individuals from the mainland. Behavioral Ecology 20: 305–312.
80. Ouyang JQ, Sharp PJ, Dawson A, Quetting M, Hau M, 2011. Hormone levels predict individual differences in reproductive success in a passerine bird. Proceedings of the Royal Society B: Biological Sciences 278: 2537–2545.
81. Parkin DT, Cole SR, 1984. Genetic variation in the house sparrow Passer domesticus in the East Midlands of England. Biological Journal of the Linnean Society 23: 287–301.
82. Parkin DT, Cole SR, 1985. Genetic differentiation and rates of evolution in some introduced populations of the house sparrow Passer domesticus in Australia and New Zealand. Heredity 54: 15–23.
83. Partecke J, Schwabl H, 2008. Organizational effects of maternal testosterone on reproductive behavior of adult house sparrows. Developmental Neurobiology 68: 1538–1548.
84. Pigliucci M, Muller GB, 2010. Evolution, the Extended Synthesis. Cambridge, MA: MIT Press.
85. Rehage JS, Sih A, 2004. Dispersal behavior, boldness, and the link to invasiveness: A comparison of four Gambusia species. Biological Invasions 6: 379–391.
86. Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M, 2006. Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters 9: 981– 993.
87. Richards CL, Schrey AW, Pigliucci M, 2012. Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation. Ecology Letters 15: 1016– 1025.
88. Richards EJ, 2006. Inherited epigenetic variation: Revisiting soft inheritance. Nature Reviews Genetics 7: 395–401.
89. Richardson DS, Dawson DA, Salgueiro P, Komdeur J, Burke T, 2000. Fifty Seychelles warbler Acrocephalus sechellensis microsatellite loci polymorphic in Sylviidae species and their cross-species amplification in other passerine birds. Molecular Ecology 9: 2226–2231.
90. Robbins CS, 1973. Introduction, spread, and present abundance of the house sparrow in North America. Ornithological Monographs 14: 3–9.
91. Russell JC, McMorland AJC, MacKay JWB, 2010. Exploratory behaviour of colonizing rats in novel environments. Animal Behaviour 79: 159–164.
92. SÆTRE GP, Riyahi S, Aliabadian M, Hermansen J, Hogner S et al., 2012. Single origin of human commensalism in the house sparrow. Journal of Evolutionary Biology 25: 788–796.
93. Schrey A, Grispo M, Awad M, Cook M, Mccoy E et al., 2011a. Broad-scale latitudinal patterns of genetic diversity among native European and introduced house sparrow Passer domesticus populations. Molecular Ecology 20: 1133–1143.
94. Schrey A, Coon CAC, Grispo M, Awad M, Imboma T et al., 2012. Epigenetic variation may compensate for decreased genetic variation with introductions: A case study using house sparrows Passer domesticus on two continents. Genetics Research International doi:10.1155/2012/979751.
95. Schrey AW, Grispo M, Awad M, Cook MB, McCoy ED et al., 2011b. Broad-scale latitudinal patterns of genetic diversity among native European and introduced house sparrow Passer domesticus populations. Molecular Ecology 20: 1133–1143.
96. Schrey AW, Liebl AL, Richards CL, Martin LB, 2014. Range expansion of house sparrows Passer domesticus in Kenya: Evidence of genetic admixture and human-mediated dispersal. Journal of Heredity 105: 60–69.
97. Shine R, Brown GP, Phillips BL, 2011. An evolutionary process that assembles phenotypes through space rather than through time. Proceedings of the National Academy of Sciences 108: 5708–5711.
98. Skinner MK, Gurerrero-Bosagna C, Haque MM, Nilsson EE, Koop JAH et al., 2014. Epigenetics and the evolution of Darwin’s finches. Genome Biology and Evolution 6: 1972–1989.
99. Skjelseth S, Ringsby TH, Tufto J, Jensen H, Sæther BE, 2007. Dispersal of introduced house sparrows Passer domesticus: An experiment. Proceedings of the Royal Society B: Biological Sciences 274: 1763–1771.
100. Slatkin M, 2009. Investigations - genetics of complex traits: Epigenetic inheritance and the missing heritability problem. Genetics 182: 845–850.
101. Sol D, Timmermans S, Lefebvre L, 2002. Behavioural flexibility and invasion success in birds. Animal Behavior 63: 495–502.
102. Stewart IR, Hanschu RD, Burke T, Westneat DF, 2006. Tests of ecological, phenotypic, and genetic correlates of extra-pair paternity in the house sparrow. The Condor 108: 399–413.
103. Tóth Z, Bókony V, Lendvai ÁZ, Szabó K, Pénzes Z et al., 2009. Kinship and aggression: Do house sparrows spare their relatives? Behavioral Ecology and Sociobiology 63: 1189–1196.
104. Väisänen RA, Lehväslaiho H, 1984. Absence of genic polymorphism in a northern population of the house sparrow Passer domesticus. Hereditas 100: 161–162.
105. Vangestel C, Mergeay J, Dawson DA, Vandomme V, Lens L, 2011a. Spatial heterogeneity in genetic relatedness among house sparrows along an urban-rural gradient as revealed by individual-based analysis. Molecular Ecology 20: 4643–4653.
106. Vangestel C, Mergeay J, Dawson DA, Vandomme V, Lens L, 2011b. Developmental stability covaries with genome-wide and single-locus heterozygosity in house sparrows. PLoS ONE. 6: e21569–e21569.
107. Vangestel C, Mergeay J, Dawson DA, Callens T, Vandomme V et al., 2012. Genetic diversity and population structure in contemporary house sparrow populations along an urbanization gradient. Heredity 109: 163–172.
108. Waddington CH, 1942. Canalization of development and the inheritance of acquired characters. Nature 150: 563–565.
109. Weaver ICG, Cervoni N, Champagne FA, D'Alessio AC, Sharma S et al., 2004. Epigenetic programming by maternal behavior. Nature Neuroscience 7: 847–854.
110. Wetton JH, Parkin DT, 1991. An association between fertility and cuckoldry in the house sparrow Passer domesticus. Proceedings of the Royal Society of London. Series B: Biological Sciences 245: 227–233.
111. Wetton JH, Parkin DT, Carter RE, 1992. The use of genetic markers for parentage analysis in Passer domesticus (house sparrows). Hereditas 69: 243–254.
112. Wetton JH, Burke T, Parkin DT, Cairns E, 1995. Single-locus DNA fingerprinting reveals that male reproductive success increases with age through extra-pair paternity in the house sparrow Passer domesticus. Proceedings of the Royal Society of London. Series B: Biological Sciences 260: 91–98.
113. Wetzel DP, Stewart IRK, Westneat DF, 2012. Heterozygosity predicts clutch and egg size but not plasticity in a house sparrow population with no evidence of inbreeding. Molecular Ecology 21: 406–420.
114. Whitekiller R, Westneat DF, Schwagmeyer P, Mock DW, 2000. Badge size and extra-pair fertilizations in the house sparrow. The Condor 102: 342–348.
115. Yeh PJ, Price TD, 2004. Adaptive phenotypic plasticity and the successful colonization of a novel environment. The American Naturalist 164: 531–542.