Distribution and population genetic variation of cryptic species of the Alpine mayfly Baetis alpinus (Ephemeroptera: Baetidae) in the Central Alps

BMC Evolutionary Biology

Volumn 16, Issue 1, 2016, Pages

  Leys, Marie ^a,b   Keller, Irene ^c   Räsänen, Katja ^a,b   Gattolliat, Jean Luc ^d,e   Robinson, Christopher T ^a,b  

^a SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF BERN   (Switzerland)

^d Musee Cantonal de Zoologie   (Switzerland)

^e UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Alpine biodiversity; Cryptic species; Mitochondrial DNA; Nuclear microsatellites; Sympatry

Indexed keywords

ALPINE ENVIRONMENT; BAYESIAN ANALYSIS; BIODIVERSITY; CLUSTER ANALYSIS; ENVIRONMENTAL ASSESSMENT; EVOLUTIONARY BIOLOGY; GENETIC MARKER; GENETIC STRUCTURE; GENETIC VARIATION; INTRASPECIFIC VARIATION; MAYFLY; MITOCHONDRIAL DNA; MORPHOLOGY; PHYLOGENETICS; POPULATION DISTRIBUTION; RELATIVE ABUNDANCE; SUBALPINE ENVIRONMENT; SYMPATRY;

ALPS; CENTRAL ALPS;

BAETIDAE; BAETIS ALPINUS; EPHEMEROPTERA;

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL DISPERSAL; BAYES THEOREM; BIODIVERSITY; CLASSIFICATION; ECOSYSTEM; EPHEMEROPTERA; EVOLUTION; GENETIC VARIATION; GENETICS; PHYLOGENY; POPULATION GENETICS; SWITZERLAND; SYMPATRY;

ANIMAL DISTRIBUTION; ANIMALS; BAYES THEOREM; BIODIVERSITY; BIOLOGICAL EVOLUTION; DNA, MITOCHONDRIAL; ECOSYSTEM; EPHEMEROPTERA; GENETIC VARIATION; GENETICS, POPULATION; MICROSATELLITE REPEATS; PHYLOGENY; SWITZERLAND; SYMPATRY;

EID: 84964982854     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/s12862-016-0643-y     Document Type: Article

References (99)

1. Via S, Gomulkiewicz R, Dejong G, Scheiner SM, Schlichting CD, Vantienderen PH. Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol. 1995;10(5):212-7.
2. Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I. Cryptic species as a window on diversity and conservation. Trends Ecol Evol. 2007;22(3):148-55.
3. Pfenninger M, Schwenk K. Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evol Biol. 2007;7:121.
4. VodǍ R, Dapporto L, DincǍ V, Vila R. Cryptic matters: overlooked species generate most butterfly beta-diversity. Ecography. 2015;38(4):405-9.
5. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK. Considering evolutionary processes in conservation biology. Trends Ecol Evol. 2000;15(7):290-5.
6. Trontelj P, Fišer C. Cryptic species diversity should not be trivialised. Syst Biodivers. 2009;7:1-3.
7. Bálint M, Domisch S, Engelhardt CHM, Haase P, Lehrian S, Sauer J, Theissinger K, Pauls SU, Nowak C. Cryptic biodiversity loss linked to global climate change. Nat Clim Chang. 2011;1(6):313-8.
8. Feckler A, Zubrod JP, Thielsch A, Schwenk K, Schulz R, Bundschuh M. Cryptic species diversity: an overlooked factor in environmental management? J Appl Ecol. 2014;51(4):958-67.
9. Macher JN, Salis RK, Blackemore KS, Tollrian R, Matthaei CD, Leese F. Multiple-stressor effects on stream invertebrates: DNA barcoding reveals contrasting responses of cryptic mayfly species. Ecol Indic. 2016;61:159-69.
10. Pauls SU, Nowak C, Bálint M, Pfenninger M. The impact of global climate change on genetic diversity within populations and species. Mol Ecol. 2013;22(4):925-46.
11. Milner AM, Brown LE, Hannah DM. Hydroecological response of river systems to shrinking glaciers. Hydrol Process. 2009;23(1):62-77.
12. Jacobsen D, Milner AM, Brown LE, Dangles O. Biodiversity under threat in glacier-fed river systems. Nat Clim Chang. 2012;2(5):361-4.
13. Cauvy-Fraunié S, Espinosa R, Andino P, Dangles O, Jacobsen D. Relationships between stream macroinvertebrate communities and new flood-based indices of glacial influence. Freshw Biol. 2014;59(9):1916-25.
14. Jackson JK, Battle JM, White BP, Pilgrim EM, Stein ED, Miller PE, Sweeney BW. Cryptic biodiversity in streams: a comparison of macroinvertebrate communities based on morphological and DNA barcode identifications. Freshwater Science. 2014;33(1):312-24.
15. Vuataz L, Sartori M, Wagner A, Monaghan MT. Toward a DNA Taxonomy of Alpine Rhithrogena (Ephemeroptera: Heptageniidae) Using a Mixed Yule Coalescent Analysis of Mitochondrial and Nuclear DNA. Plos One. 2011;6(5):e19728.
16. Rutschmann S, Gattolliat J-L, Hughes SJ, Baez M, Sartori M, Monaghan MT. Evolution and island endemism of morphologically cryptic Baetis and Cloeon species (Ephemeroptera, Baetidae) on the Canary Islands and Madeira. Freshw Biol. 2014;59:2516-27.
17. Sroka P, Godunko RJ, Novikova EA, Kluge NJ. Contribution to the knowledge of the subgenus Rhodobaetis Jacob, 2003 (Ephemeroptera: Baetidae: Baetis) from Central Asia. Part 1. Zootaxa. 2012;3311:42-60.
18. Hughes JM, Mather PB, Hillyer MJ, Cleary C, Peckarsky B. Genetic structure in a montane mayfly Baetis bicaudatus (Ephemeroptera: Baetidae), from the Rocky Mountains, Colorado. Freshw Biol. 2003;48(12):2149-62.
19. Williams HC, Ormerod SJ, Bruford MW. Molecular systematics and phylogeography of the cryptic species complex Baetis rhodani (Ephemeroptera, Baetidae). Mol Phylogenet Evol. 2006;40(2):370-82.
20. Stahls G, Savolainen E. MtDNA COI barcodes reveal cryptic diversity in the Baetis vernus group (Ephemeroptera, Baetidae). Mol Phylogenet Evol. 2008;46(1):82-7.
21. Pereira-da-Conceicoa LL, Price BW, Barber-James HM, Barker NP, de Moor FC, Villet MH. Cryptic variation in an ecological indicator organism: mitochondrial and nuclear DNA sequence data confirm distinct lineages of Baetis harrisoni Barnard (Ephemeroptera: Baetidae) in southern Africa. BMC Evol Biol. 2012;12:26.
22. Finn DS, Khamis K, Milner AM. Loss of small glaciers will diminish beta diversity in Pyrenean streams at two levels of biological organization. Glob Ecol Biogeogr. 2013;22(1):40-51.
23. Finn DS, Zamora-Muñoz C, Múrria C, Sáinz-Bariáin M, Alba-Tercedor J. Evidence from recently deglaciated mountain ranges that Baetis alpinus (Ephemeroptera) could lose significant genetic diversity as alpine glaciers disappear. Freshwater Science. 2014;33(1):207-16.
24. Múrria C, Morante M, Rieradevall M, Ribera C, Prat N. Genetic diversity and species richness patterns in Baetidae (Ephemeroptera) in the Montseny Mountain range (North-East Iberian Peninsula). Limnetica. 2014;33(2):313-26.
25. Gattolliat J-L, Cavallo E, Vuataz L, Sartori M. DNA barcoding of Corsican mayflies (Ephemeroptera) with implications on biogeography, systematics and biodiversity. Arthropod Systematics Phylogeny. 2015;73(1):3-18.
26. Lepori F, Ormerod SJ. Effects of spring acid episodes on macroinvertebrates revealed by population data and in situ toxicity tests. Freshw Biol. 2005;50(9):1568-77.
27. Dijkstra KDB, Monaghan MT, Pauls SU. Freshwater biodiversity and aquatic insect diversification. Annu Rev Entomol. 2014;59:143-63.
28. De Queiroz K. Species concepts and species delimitation. Syst Biol. 2007;56(6):879-86.
29. Mallet J. A species definition for the modern synthesis. Trends Ecol Evol. 1995;10(7):294-9.
30. Hebert PDN, Cywinska A, Ball SL, DeWaard JR. Biological identifications through DNA barcodes. Proc R Soc B-Biol Sci. 2003;270(1512):313-21.
31. Ball SL, Hebert PDN, Burian SK, Webb JM. Biological identifications of mayflies (Ephemeroptera) using DNA barcodes. J N Am Benthol Soc. 2005;24(3):508-24.
32. Bensasson D, Zhang DX, Hartl DL, Hewitt GM. Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends Ecol Evol. 2001;16(6):314-21.
33. Ballard JWO, Whitlock MC. The incomplete natural history of mitochondria. Mol Ecol. 2004;13(4):729-44.
34. Funk DJ, Omland KE. Species-level paraphyly and polyphyly: Frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Evol Syst. 2003;34:397-423.
35. Toews DPL, Brelsford A. The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol. 2012;21(16):3907-30.
36. Cheng S, Lee CT, Wan MN, Tan SG. Microsatellite markers uncover cryptic species of Odontotermes (Termitoidae: Termitidae) from Peninsular Malaysia. Gene. 2013;518(2):412-8.
37. Hoekzema K, Sidlauskas BL. Molecular phylogenetics and microsatellite analysis reveal cryptic species of speckled dace (Cyprinidae: Rhinichthys osculus) in Oregon's Great Basin. Mol Phylogenet Evol. 2014;77:238-50.
38. Andrews KR, Norton EL, Fernandez-Silva I, Portner E, Goetze E. Multilocus evidence for globally distributed cryptic species and distinct populations across ocean gyres in a mesopelagic copepod. Mol Ecol. 2014;23(22):5462-79.
39. Wang H-L, Yang J, Boykin LM, Zhao Q-Y, Wang Y-J, Liu S-S, Wang X-W. Developing conversed microsatellite markers and their implications in evolutionary analysis of the Bemisia tabaci complex. Sci Rep. 2014;4:6351.
40. Racey PA, Barratt EM, Burland TM, Deaville R, Gotelli D, Jones G, Piertney SB. Microsatellite DNA polymorphism confirms reproductive isolation and reveals differences in population genetic structure of cryptic pipistrelle bat species. Biol J Linn Soc. 2007;90(3):539-50.
41. Westram AM, Jokela J, Keller I. Hidden biodiversity in an ecologically important freshwater amphipod: differences in genetic structure between two cryptic species. Plos One. 2013;8(8):e69576.
42. Knispel S, Sartori M, Brittain JE. Egg development in the mayflies of a Swiss glacial floodplain. J N Am Benthol Soc. 2006;25(2):430-43.
43. Humpesch UH. Life cycles and growth rates of Baetis spp. (Ephemeroptera: Baetidae) in the laboratory and in two stony streams in Austria. Freshw Biol. 1979;9(5):467-79.
44. Schmidt SK, Hughes JM, Bunn SE. Gene flow among conspecific populations of Baetis sp. (Ephemeroptera): adult flight and larval drift. J N Am Benthol Soc. 1995;14(1):147-57.
45. Müller-Liebenau I. Revision der europaischen Arten der Gattung Baetis Leach, 1815 (Insecta, Ephemeroptera). Gewässer und Abwässer. 1969;48/49:1-214.
46. Bauernfeind E, Soldan T. The mayflies of Europe (Ephemeroptera). Ollerup, Denmark: Appollo Books; 2012.
47. Thomas AGB, Gazagnes G. Baetis cyrneus n. sp., Ephéméroptère nouveau de Corse (Baetidae). Ann Limnol. 1984;20(3):199-202.
48. Sartori M. New records and redescription of Baetis nubecularis Eaton, 1898 from the Swiss Jura (Ephemeroptera, Baetidae). Aquat Insects. 1985;7(4):209-14.
49. Breitenmoser-Würsten C, Sartori M. Distribution, diversity, life cycle and growth of a mayfly community in a prealpine stream system (Insecta, Ephemeroptera). Hydrobiologia. 1995;308(2):85-101.
50. Lavandier P. Evidence of upstream migration by female adults of Baetis alpinus (Ephemeroptera) at high altitude in the Pyrenees. Ann Limnol. 1982;18(1):55-60.
51. Lavandier P. Semivoltinism in high mountain populations of Baetis alpinus Pictet. (Ephemeroptera). Bulletin de la Société d'Histoire Naturelle de Toulouse. 1988;124:61-4.
52. Kukula K. The life cycles of three species of Ephemeroptera in two streams in Poland. Hydrobiologia. 1997;353:193-8.
53. Erba S, Melissano L, Buffagni A. Life cycles of Baetidae (Insecta: Ephemeroptera) in a North Italian Prealpine stream. In: Gaino E, editor. Research update on Ephemeroptera and Plecoptera. Perugia, Italy: University of Perugia Press; 2003. p. 177-86.
54. López-Rodríguez MJ, de Figueroa JMT, Alba-Tercedor J. Life history and larval feeding of some species of Ephemeroptera and Plecoptera (Insecta) in the Sierra Nevada (Southern Iberian Peninsula). Hydrobiologia. 2008;610:277-95.
55. Ward JV, Stanford JA. Thermal responses in the evolutionary ecology of aquatic insects. Annu Rev Entomol. 1982;27:97-117.
56. Sartori M, Landolt P. Atlas de distribution des éphémères de Suisse (Insecta, Ephemeroptera), vol. 3. Neuchâtel, Switzerland: SEG-CSCF; 1999.
57. Studemann D, Landolt P, Sartori M, Hefti D, Tomka I. Ephemeroptera. Insecta helvetica, Fauna 9. Fribourg, Switzerland: Imprimerie Mauron, Tinguely and Lachat SA; 1992.
58. Ward JV, Malard F, Tockner K, Uehlinger U. Influence of ground water on surface water conditions in a glacial flood plain of the Swiss Alps. Hydrol Process. 1999;13(3):277-93.
59. Füreder L, Schütz C, Wallinger M, Burger R. Physico-chemistry and aquatic insects of a glacier-fed and a spring-fed alpine stream. Freshw Biol. 2001;46(12):1673-90.
60. Bauernfeind E, Humpesch UH. Die Eintagsfliegen Zentraleuropas (Insecta: Ephemeroptera): Bestimmung und Oekologie. Wien, Austria: Verlag des Naturhistorischen Museums Wien; 2001.
61. Sunnucks P, England PR, Taylor AC, Hales DF. Microsatellite and chromosome evolution of parthenogenetic Sitobion aphids in Australia. Genetics. 1996;144(2):747-56.
62. Dawson DA, Horsburgh GJ, Kupper C, Stewart IRK, Ball AD, Durrant KL, Hansson B, Bacon I, Bird S, Klein A, et al. New methods to identify conserved microsatellite loci and develop primer sets of high cross-species utility - as demonstrated for birds. Mol Ecol Resour. 2010;10(3):475-94.
63. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3(5):294-9.
64. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95-8.
65. Goudet J. FSTAT (Version 1.2): A computer program to calculate F-statistics. J Hered. 1995;86(6):485-6.
66. Raymond M, Rousset F. GENEPOP (Version-1.2) - Population genetics software for exact tests and ecumenicism. J Hered. 1995;86(3):248-9.
67. Dempster AP, Laird NM, Rubin DB. Maximum Likelihood from incomplete data via the EM Algorithm. J R Stat Soc Ser B Methodol. 1977;39:1-38.
68. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155(2):945-59.
69. Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics. 2003;164(4):1567-87.
70. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14(8):2611-20.
71. Meirmans PG. Seven common mistakes in population genetics and how to avoid them. Mol Ecol. 2015;24(13):3223-31.
72. Jakobsson M, Rosenberg NA. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007;23(14):1801-6.
73. Rosenberg NA. DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes. 2004;4(1):137-8.
74. Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 2010;11:94.
75. Jombart T. ADEGENET: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24(11):1403-5.
76. Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics. 2004;20(2):289-90.
77. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52(5):696-704.
78. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM. Mixed effects models and extensions in ecology with R. New York: Springer; 2009.
79. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2015.
80. Jombart T, Devillard S, Dufour AB, Pontier D. Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity. 2008;101(1):92-103.
81. Frantz AC, Cellina S, Krier A, Schley L, Burke T. Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? J Appl Ecol. 2009;46(2):493-505.
82. Schwartz MK, McKelvey KS. Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet. 2009;10(2):441-52.
83. Menozzi P, Piazza A, Cavalli-Sforza L. Synthetic maps of human gene-frequencies in Europeans. Science. 1978;201(4358):786-92.
84. Weir BS, Cockerham CC. Estimating F-statistics for the analysis of population structure. Evolution. 1984;38(6):1358-70.
85. El Mousadik A, Petit RJ. High level of genetic differentiation for allelic richness among populations of the argan tree Argania spinosa (L) Skeels endemic to Morocco. Theor Appl Genet. 1996;92(7):832-9.
86. Szpiech ZA, Jakobsson M, Rosenberg NA. ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics. 2008;24(21):2498-504.
87. Siegel S, Castellan NJ. Non parametric statistics for the behavioural sciences. New York: MacGraw Hill Int; 1988.
88. Peru N, Thomas A. Compléments et corrections à la faune des Ephéméroptères d'Afrique du Nord. 7. Description complémentaire de Baetis berberus Thomas, 1986 (Ephemeroptera, Baetidae). Ephemera. 2003;3(2):75-82.
89. Hewitt GM. Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc Lond Ser B Biol Sci. 2004;359(1442):183-95.
90. Coyne JA, Orr HA. Speciation. Sunderland, MA: Sinauer Associates; 2004.
91. Sota T, Kubota K. Genital lock-and-key as a selective agent against hybridization. Evolution. 1998;52(5):1507-13.
92. Savolainen E, Saura A, Hantula J. Mode of swarming in relation to reproductive isolation in mayflies. Evolution. 1993;47(6):1796-804.
93. Seehausen O, Butlin RK, Keller I, Wagner CE, Boughman JW, Hohenlohe PA, Peichel CL, Saetre G-P, Bank C, Braennstroem A. Genomics and the origin of species. Nat Rev Genet. 2014;15(3):176-92.
94. Chesson P. Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst. 2000;31:343-66.
95. Wagner A, Sartori M. Liste rouge des Ephémères de Suisse. In: Lubini V, Knispel S, Sartori M, Vicentini FL, Wagner A, editors. Listes rouges Ephémères, Plécoptères Trichoptères: Espèces menacées en Suisse, état 2010. Bern: Office fédéral de l'Environnement & Centre Suisse de Cartographie de la Faune; 2012.
96. Caudill CC. Empirical evidence for nonselective recruitment and a source-sink dynamic in a mayfly metapopulation. Ecology. 2003;84(8):2119-32.
97. Bunn SE, Hughes JM. Dispersal and recruitment in streams: Evidence from genetic studies. J N Am Benthol Soc. 1997;16(2):338-46.
98. Bohonak AJ, Jenkins DG. Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecol Lett. 2003;6(8):783-96.
99. Elbrecht V, Feld CK, Gies M, Hering D, Sondermann M, Tollrian R, Leese F. Genetic diversity and dispersal potential of the stonefly Dinocras cephalotes in a central European low mountain range. Freshwater Science. 2014;33(1):181-91.