Biological Invasions

, Volume 17, Issue 1, pp 123–132 | Cite as

Ecological limits can obscure expansion history: patterns of genetic diversity in a temperate mosquito in Hawaii

Original Paper

Abstract

Because biological invasions can be swift and are rarely examined immediately and/or followed over time, spatial genetic diversity analyses grounded in a well-developed body of theory are often used to reconstruct historical patterns of expansion. Unfortunately, the role of selection in shaping and potentially disrupting such reconstructions has seldom been examined. The mosquito Aedes japonicus japonicus is a temperate, cold-adapted species native to northern Japan that has recently established populations on the island of Hawaii. We used variation at seven microsatellite loci and one mitochondrial locus to examine Hawaiian populations collected in 2004, shortly after its first detection, and then in 2010–2011. Samples were collected along an elevational/temperature gradient, ranging from sea level to 1,200 m. Specimens collected near sea level in 2004 from the earliest detected population exhibited high genetic diversity. Contrary to expectations that diversity would decrease outward from the point of introduction, in 2010–2011 high elevation populations had the greatest genetic diversity, while low elevation populations (including those with high diversity in 2004) now had lower diversity and were significantly differentiated from each other, suggesting severe bottlenecks. We hypothesize that differential survival across temperatures at high versus low elevations has subverted the expected genetic signature of an expanding population.

Keywords

Spatial genetics Invasion genetics Elevation Temperature tolerance Natural selection Rapid evolution 

References

  1. Amsellem L, Noyer JL, Le Bourgeois T et al (2000) Comparison of genetic diversity of the invasive weed Rubus alceifolius poir. (Rosaceae) in its native range and in areas of introduction, using amplified fragment length polymorphism (AFLP) markers. Mol Ecol 9:443–455PubMedCrossRefGoogle Scholar
  2. Austerlitz F, Jung-Muller B, Godelle B et al (1997) Evolution of coalescence times, genetic diversity and structure during colonization. Theor Popul Biol 51:148–164CrossRefGoogle Scholar
  3. Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central–marginal hypothesis and beyond. Mol Ecol 17:1170–1188PubMedCrossRefGoogle Scholar
  4. Egizi A, Morin PJ, Fonseca DM (2014) Unraveling microbe-mediated interactions between mosquito larvae in a laboratory microcosm. Aquat Ecol 48:179–189Google Scholar
  5. Estoup A, Beaumont M, Sennedot F et al (2004) Genetic analysis of complex demographic scenarios: spatially expanding populations of the cane toad, Bufo marinus. Evolution 58:2021–2036PubMedCrossRefGoogle Scholar
  6. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  7. Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864PubMedCrossRefGoogle Scholar
  8. Excoffier L, Foll M, Petit RJ (2008) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501CrossRefGoogle Scholar
  9. Fitzpatrick B, Fordyce J, Niemiller M et al (2012) What can DNA tell us about biological invasions? Biol Invasions 14:245–253CrossRefGoogle Scholar
  10. Foll M, Gaggiotti O (2006) Identifying the environmental factors that determine the genetic structure of populations. Genetics 174:875–891Google Scholar
  11. Fonseca DM, Campbell S, Crans WJ et al (2001) Aedes (Finlaya) japonicus (Diptera: Culicidae), a newly recognized mosquito in the United States: analyses of genetic variation in the United States and putative source populations. J Med Entomol 38:135–146PubMedCrossRefGoogle Scholar
  12. Fonseca DM, Widdel AK, Hutchinson M et al (2010) Fine-scale spatial and temporal population genetics of Aedes japonicus, a new US mosquito, reveal multiple introductions. Mol Ecol 19:1559–1572PubMedCrossRefGoogle Scholar
  13. Fonseca DM, Kaplan LR, Heiry RA, et al. (2014) Studies of ovipositing Aedes albopictus reveal a highly adaptable and risk-averse invader. Med Vet Entomol, acceptedGoogle Scholar
  14. Funk WC, Blouin MS, Corn PS et al (2005) Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Mol Ecol 14:483–496PubMedCrossRefGoogle Scholar
  15. Gaggiotti O, Foll M (2010) Quantifying population structure using the F-model. Mol Ecol Res 10:821–830Google Scholar
  16. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-Statistics. J Hered 86:485–486Google Scholar
  17. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638PubMedCrossRefGoogle Scholar
  18. Herborg LM, Weetman D, van Oosterhout C et al (2007) Genetic population structure and contemporary dispersal patterns of a recent European invader, the Chinese mitten crab, Eriocheir sinensis. Mol Ecol 16:231–242PubMedCrossRefGoogle Scholar
  19. Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913PubMedCrossRefGoogle Scholar
  20. Huey RB, Gilchrist GW, Carlson ML et al (2000) Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308–309PubMedCrossRefGoogle Scholar
  21. Kaufman MG, Fonseca DM (2014) Invasion biology of Aedes japonicus japonicus (Diptera: Culicidae). Annu Rev Entomol 59:31–49Google Scholar
  22. Keyghobadi N, Lapointe D, Fleischer RC et al (2006) Fine-scale population genetic structure of a wildlife disease vector: the southern house mosquito on the island of Hawaii. Mol Ecol 15:3919–3930PubMedCrossRefGoogle Scholar
  23. LaPointe DA (2006) Feral pigs, introduced mosquitoes, and the decline of Hawaiian birds. U.S. Geological Survey Fact Sheet 2006–3029Google Scholar
  24. Larish LB, Savage HM (2005) Introduction and establishment of Aedes (Finlaya) japonicus japonicus (Theobald) on the island of Hawaii: implications for arbovirus transmission. J Am Mosq Control Assoc 21:318–321PubMedCrossRefGoogle Scholar
  25. Larish LB, Yang P, Asuncion BA (2010) Distribution and abundance of Aedes (Finlaya) japonicus japonicus (Theobald) in five districts on the island of Hawaii. Proc Hawaii Entomol Soc 42:9–14Google Scholar
  26. Le Corre V, Kremer A (1998) Cumulative effects of founding events during colonisation on genetic diversity and differentiation in an island and stepping-stone model. J Evol Biol 11:495–512CrossRefGoogle Scholar
  27. Leberg PL (2002) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11:2445–2449PubMedCrossRefGoogle Scholar
  28. Liebherr JK (1986) Comparison of genetic variation in two Carabid beetles (Coleoptera) of differing vagility. Ann Entomol Soc Am 79:424–433Google Scholar
  29. Lozier JD, Strange JP, Stewart IJ et al (2011) Patterns of range-wide genetic variation in six North American bumble bee (Apidae: Bombus) species. Mol Ecol 20:4870–4888PubMedCrossRefGoogle Scholar
  30. Mayr E (1942) Systematics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  31. Mestres F, Abad L, Sabater-Muñoz B et al (2004) Colonization of America by Drosophila subobscura: association between Odh gene haplotypes, lethal genes and chromosomal arrangements. Genes Genet Syst 79:233–244PubMedCrossRefGoogle Scholar
  32. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  33. Ohsawa T, Ide Y (2008) Global patterns of genetic variation in plant species along vertical and horizontal gradients on mountains. Glob Ecol Biogeogr 17:152–163CrossRefGoogle Scholar
  34. Oksanen J, Blanchet FG, Kindt R et al. (2013) Vegan: community ecology package. R package version 2.0-7Google Scholar
  35. Peakall ROD, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  36. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel: population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539PubMedCentralPubMedCrossRefGoogle Scholar
  37. Peyton EL, Campbell SR, Candeletti TM et al (1999) Aedes (Finlaya) japonicus japonicus (Theobald), a new introduction into the United States. J Am Mosq Control Assoc 15:238–241PubMedGoogle Scholar
  38. Potvin C, Simon J-P, Strain B (1986) Effect of low temperature on the photosynthetic metabolism of the C4 grass Echinochloa crus-galli. Oecologia 69:499–506CrossRefGoogle Scholar
  39. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  40. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  41. Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86PubMedCrossRefGoogle Scholar
  42. Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  43. Reiter P (2007) Oviposition, dispersal, and survival in Aedes aegypti: implications for the efficacy of control strategies. Vector Borne Zoonotic Dis 7:261–273PubMedCrossRefGoogle Scholar
  44. Roppo MR, Lilja JL, Maloney FA et al (2004) First occurrence of Ochlerotatus japonicus in the state of Washington. J Am Mosq Control Assoc 20:83–84PubMedGoogle Scholar
  45. Roy S, Simon JP, Lapointe FJ (2000) Determination of the origin of the cold-adapted populations of barnyard grass (Echinochloa crusgalli) in eastern North America: a total-evidence approach using RAPD DNA and DNA sequences. Can J Bot. Journal canadien de botanique 78:1505–1513CrossRefGoogle Scholar
  46. Schaffner F, Kaufmann C, Hegglin D et al (2009) The invasive mosquito Aedes japonicus in Central Europe. Med Vet Entomol 23:448–451PubMedCrossRefGoogle Scholar
  47. Schiffer M, Kennington WJ, Hoffmann AA et al (2007) Lack of genetic structure among ecologically adapted populations of an Australian rainforest Drosophila species as indicated by microsatellite markers and mitochondrial DNA sequences. Mol Ecol 16:1687–1700PubMedCrossRefGoogle Scholar
  48. Schulte U, Veith M, Mingo V et al. (2013) Strong genetic differentiation due to multiple founder events during a recent range expansion of an introduced wall lizard population. Biol Invasions 15:2639–2649Google Scholar
  49. Scott JJ (2003) The ecology of the exotic mosquito Ochlerotatus (Finlay) japonicus japonicus (Theobald 1901) (Diptera: Culicidae) and an examination of its role in the West Nile virus cycle in New Jersey. Department of Entomology. Rutgers UniversityGoogle Scholar
  50. Sherwin WB (2010) Entropy and information approaches to genetic diversity and its expression: genomic geography. Entropy 12:1765–1798CrossRefGoogle Scholar
  51. Sherwin WB, Jabot F, Rush R et al (2006) Measurement of biological information with applications from genes to landscapes. Mol Ecol 15:2857–2869PubMedCrossRefGoogle Scholar
  52. Short KH, Petren K (2011) Fine-scale genetic structure arises during range expansion of an invasive gecko. PLoS One 6:e26258PubMedCentralPubMedCrossRefGoogle Scholar
  53. Spear SF, Peterson CR, Matocq MD et al (2005) Landscape genetics of the blotched tiger salamander (Ambystoma tigrinum melanostictum). Mol Ecol 14:2553–2564PubMedCrossRefGoogle Scholar
  54. Tanaka K, Mizusawa K, Saugstad ES (1979) A revision of the adult and larval mosquitoes of Japan (including the Ryukyu Archipelago and the Ogasawara islands) and Korea (Diptera:Culicidae). Contrib Am Entomol Inst 16:1–987Google Scholar
  55. Thielman A, Hunter FF (2006) Establishment of Ochlerotatus japonicus (Diptera: Culicidae) in Ontario, Canada. J Med Entomol 43:138–142PubMedCrossRefGoogle Scholar
  56. Urbanski J, Mogi M, O’Donnell D et al (2012) Rapid adaptive evolution of photoperiodic response during invasion and range expansion across a climatic gradient. Am Nat 179:490–500PubMedCrossRefGoogle Scholar
  57. Wegmann D, Currat M, Excoffier L (2006) Molecular diversity after a range expansion in heterogeneous environments. Genetics 174:2009–2020PubMedCentralPubMedCrossRefGoogle Scholar
  58. Wen CS, Hsiao JY (2001) Altitudinal genetic differentiation and diversity of Taiwan Lily (Lilium longiflorum var. formosanum; Liliaceae) using RAPD markers and morphological characters. Int J Plant Sci 162:287–295CrossRefGoogle Scholar
  59. Widdel AK, McCuiston LJ, Crans WJ et al (2005) Finding needles in the haystack: single copy microsatellite loci for Aedes japonicus (Diptera: Culicidae). Am J Trop Med Hyg 73:744–748PubMedGoogle Scholar
  60. Williams CK, Moore RJ (1989) Phenotypic adaptation and natural selection in the wild rabbit, Oryctolagus cuniculus, in Australia. J Anim Ecol 58:495–507CrossRefGoogle Scholar
  61. Zielke DE, Werner D, Kampen H et al. (2014) Unexpected patterns of admixture in German populations of Aedes japonicus japonicus (Diptera: Culicidae) underscore the importance of human intervention. PLoS One, acceptedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Department of Entomology, Center for Vector BiologyRutgers UniversityNew BrunswickUSA
  2. 2.Graduate Program in Ecology and EvolutionRutgers UniversityNew BrunswickUSA

Personalised recommendations