Genetic variation across trophic levels: A test of the correlation between population size and genetic diversity in sympatric desert lizards


Autoři: Erica M. Rutherford aff001;  Andrew Ontano aff001;  Camille Kantor aff001;  Eric J. Routman aff001
Působiště autorů: Department of Biology, San Francisco State University, Holloway Avenue, San Francisco, California, United States of America aff001
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pone.0224040

Souhrn

Understanding the causes of genetic variation in real populations has been elusive. Competing theories claim that neutral vs. selective processes have a greater influence on the genetic variation within a population. A key difference among theories is the relationship between population size and genetic diversity. Our study tests this empirically by sampling two species of herbivorous lizards (Dipsosaurus dorsalis and Sauromalus ater) and two species of carnivorous lizards (Crotaphytus bicinctores and Gambelia wislizenii) that vary in population size at the same locality, and comparing metrics of genetic diversity. Contrary to neutral expectations, results from four independent loci showed levels of diversity were usually higher for species with smaller population sizes. This suggests that selective processes may be having an important impact on intraspecific diversity in this reptile community, although tests showed little evidence for selection on the loci sequenced for this study. It is also possible that idiosyncratic histories of the focal species may be overriding predictions from simple neutral models. If future studies show that lack of correlation between population size and genetic diversity is common, methods using genetic diversity to estimate population parameters like population size or time to common ancestor should be used with caution, as these estimates are based on neutral theory predictions.

Klíčová slova:

Genetic loci – Haplotypes – Lizards – Phylogeography – Population genetics – Population size – Species diversity – Reptile genetics


Zdroje

1. Kimura M. The neutral theory of molecular evolution. Cambridge: Cambridge University Press; 1983.

2. Frankham R. How closely does genetic diversity in finite populations conform to predictions of neutral theory? Large deficits in regions of low recombination. Heredity. 2011 Aug 21;108:167–178. doi: 10.1038/hdy.2011.66 21878983

3. Lynch M, Conery JS. The origins of genome complexity. Science. 2003 Nov 21;302(5649):1401–1404. doi: 10.1126/science.1089370 14631042

4. McCusker MR, Bentzen P. Positive relationships between genetic diversity and abundance in fishes. Mol Ecol. 2010 Sep 17;19(22):4852–4862. doi: 10.1111/j.1365-294X.2010.04822.x 20849560

5. Nei M, Suzuki Y, Nozawa M. The neutral theory of molecular evolution in the genomic era. Annu Rev Genomics Hum Genet. 2010 Sep 22;11:265–289. doi: 10.1146/annurev-genom-082908-150129 20565254

6. Amos W, Harwood J. Factors affecting levels of genetic diversity in natural populations. Philos Trans R Soc Lond B. 1998 Feb 28;353(1366):177–186.

7. Bazin E, Glémin S, Galtier N. Population size does not influence mitochondrial genetic diversity in animals. Science. 2006 Apr 28;312(5773):570–572. doi: 10.1126/science.1122033 16645093

8. Kern AD, Hahn MW. The neutral theory in light of natural selection. Mol. Biol. Evol. 2018;35(6):1366–1371. doi: 10.1093/molbev/msy092 29722831

9. Ohta T. The nearly neutral theory of molecular evolution. Annu Rev Ecol Syst. 1992 Nov;23:263–286.

10. Gillespie JH. The neutral theory in an infinite population. Gene. 2000 Dec 30;261(1):11–18. doi: 10.1016/s0378-1119(00)00485-6 11164032

11. Gillespie JH. Is the population size of a species relevant to its evolution? Evolution. 2001 Dec;55(11):2161–2169. doi: 10.1111/j.0014-3820.2001.tb00732.x 11794777

12. Charlesworth B, Nordborg M, Charlesworth D. The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet Res. 1997 Oct 01;70(2):155–174. doi: 10.1017/s0016672397002954 9449192

13. Corbett-Detig RB, Hartl DL, Sackton TB. Natural selection constrains neutral diversity across a wide range of species. PLoS Biol. 2015 Apr 10; doi: 10.1371/journal.pbio.1002112 25859758

14. Frankham R. Relationship of genetic variation to population size in wildlife. Conserv Biol. 1996 Dec;10(6): 1500–1508.

15. Lanfear R, Kokko H, Eyre-Walker A. Population size and the rate of evolution. Trends Ecol Evol. 2014 Jan;29(1):33–41. doi: 10.1016/j.tree.2013.09.009 24148292

16. Ellegren H, Galtier N. Determinants of genetic diversity. Nat Rev Genet. 2016 Jul 6;17:422–433. doi: 10.1038/nrg.2016.58 27265362

17. Romiguier J, Gayral P, Ballenghien M, Bernard A, Cahais V, Chenuil A et. al. Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature. 2014 Nov 13;515:261–263. doi: 10.1038/nature13685 25141177

18. Figuet E, Nabholz B, Bonneau M, Mas Carrio E, Nadachowska-Brzyska K, Ellegren H, Galtier N. Life history traits, protein evolution, and the nearly neutral theory in amniotes. Mol Biol Evol. 04 Mar 2016;33(6):1517–1527. doi: 10.1093/molbev/msw033 26944704

19. Micheletti S, Parra E, Routman EJ. Adaptive color polymorphism and unusually high local genetic diversity in the Side-Blotched Lizard, Uta stansburiana. PLoS One. 2012 Oct 25;7(10):e47694. doi: 10.1371/journal.pone.0047694 23133520

20. Hague MTJ, Routman EJ. Does population size affect genetic diversity? A test with sympatric lizard species. Heredity. 2015 Aug 26;116:92–98. doi: 10.1038/hdy.2015.76 26306730

21. Wiens JJ, Hutter CR, Mulcahy DG, Noonan BP, Townsend TM, Sites JW Jr., et. al. Resolving the phylogeny of lizards and snakes (Squamata) with extensive sampling of genes and species. Biol Lett. 2012 Sep 19;rsbl20120703.

22. Pyron RA, Burbrink FT, Wiens JJ. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol. 2013 Apr 29;13(93): 1–53.

23. Hollingsworth BD. Long-nosed Leopard Lizard. In: Jones LLC, Lovich RE, editors. Lizards of the American Southwest: A photographic field guide. Tucson (AZ): Rio Nuevo Publishers; 2009. p. 124–127.

24. Ryan MJ. Great Basin Collared Lizard. In: Jones LLC, Lovich RE, editors. Lizards of the American Southwest: A photographic field guide. Tucson (AZ): Rio Nuevo Publishers; 2009. p. 100–103.

25. Kwiatkowski MA, Jones LLC, Sullivan BK. Common Chuckwalla. In: Jones LLC, Lovich RE, editors. Lizards of the American Southwest: A photographic field guide. Tucson (AZ): Rio Nuevo Publishers; 2009. p. 135–138.

26. Lemm JM. Desert Iguana. In: Jones LLC, Lovich RE, editors. Lizards of the American Southwest: A photographic field guide. Tucson (AZ): Rio Nuevo Publishers; 2009. p. 131–134.

27. Wallace JK. Population abundance and diversity of reptiles in the East Mojave, Soda Springs Area [thesis]. Fullerton (CA): California State University, Fullerton; 2003.

28. Persons TB, Nowak EM. Inventory of Amphibians and Reptiles at Mojave National Preserve. Final report. U.S. Geological Survey; 2007. Open-File Report No.:2007–1109.

29. Avise JC, Bowen BW, Lamb T. DNA Fingerprints from hypervariable mitochondrial genotypes. Mol Biol Evol. 1989 May 01;6(3):258–269. doi: 10.1093/oxfordjournals.molbev.a040546 2576092

30. Lamb T, Jones TR, Avise JC. Phylogeographic histories of representative herpetofauna of the southwestern U.S.: mitochondrial DNA variation in the desert iguana (Dipsosaurus dorsalis) and the chuckwalla (Sauromalus obesus). J Evol Biol. 1992 May;5(3):465–480.

31. Orange DI, Riddle BR, Nickle DC. Phylogeography of a wide-ranging desert lizard, Gambelia wislizenii (Crotaphytidae). Copeia. 1999 May 7;1999(2):267–273.

32. McGuire JA, Linkem CW, Koo MS, Hutchison DW, Lappin AK, Orange DI, et. al. Mitochondrial introgression and incomplete lineage sorting through space and time: Phylogenetics of crotaphytid lizards. Evolution. 2007 Oct 10;61(12):2879–2897. doi: 10.1111/j.1558-5646.2007.00239.x 17941840

33. Robinson JG, and Redford KH. Body size, diet, and population density of neotropical forest mammals. The American Naturalist 1986 Nov 128(5) 665–680.

34. Jonsson T, Cohen JE, Carpenter SR. Food webs, body size, and species abundance in ecological community description. Adv Ecol Res. 2005 36:1–84.

35. Cummings KL, Puffer SR, Holmen JB, Wallace JK, Lovich JE, Meyer-Wilkins K. Biodiversity of amphibians and reptiles at the Camp Cady Wildlife Area, Mojave Desert, California and comparisons with other desert locations. California Fish and Game 2018 Summer 104(3): 129–147.

36. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et. al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012 Apr 27;28(12):1647–1649. doi: 10.1093/bioinformatics/bts199 22543367

37. Stephens M, Smith NJ, Donnelly P. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet. 2001 Apr;68(4):978–989. doi: 10.1086/319501 11254454

38. Stephens M, Donnelly P. A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet. 2003 Nov;73(5):1162–1169. doi: 10.1086/379378 14574645

39. Flot JF. SEQPHASE: a web tool for interconverting phase input/output files and fasta sequence alignments. Mol Ecol. Resour. 2009 Dec 16;10(1):162–166. doi: 10.1111/j.1755-0998.2009.02732.x 21565002

40. R Core Team. R: A language and environment for statistical computing [software]. 2014. R Foundation for Statistical Computing, Vienna, Austria. Available from: http://www.R-project.org/.

41. Excoffier L, Lischer HEL. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010 Apr 6;10(3):564–567. doi: 10.1111/j.1755-0998.2010.02847.x 21565059

42. Watterson G. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. doi: 10.1016/0040-5809(75)90020-9 1145509

43. Tajima F. The effect of change in population size on DNA polymorphism. Genetics. 1989 Nov 1;123(3):597–601. 2599369

44. Cumming G, Finch S. Inference by eye: confidence intervals and how to read pictures of data. Am Psychol. 2005 Feb;60(2):170–180. doi: 10.1037/0003-066X.60.2.170 15740449

45. Librado P, Rozas J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009 Apr 3;25(11):1451–1452. doi: 10.1093/bioinformatics/btp187 19346325

46. Nei M. Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci U S A. 1973 Dec 1;70(12):3321–3323. doi: 10.1073/pnas.70.12.3321 4519626

47. Nei M, Chesser RK. Estimation of fixation indices and gene diversities. Ann Hum Genet. 1983 Jul;47(3):253–259. doi: 10.1111/j.1469-1809.1983.tb00993.x 6614868

48. Jost L. GST and its relatives do not measure differentiation. Mol Ecol. 2008 Sep 26;17(18):4015–4026. doi: 10.1111/j.1365-294x.2008.03887.x 19238703

49. Schou MF, Loeschcke V, Bechsgaard J, Schlötterer C, Kristensen TN. Unexpected high genetic diversity in small populations suggests maintenance by associative overdominance. Mole Ecol. 2017 Jun 28;26:6510–6523.

50. Weissman DB, Hallatschek O. Minimal-assumption inference from population-genomic data. eLife. 2017 Jul 3;6:e24836. doi: 10.7554/eLife.24836 28671549

51. Grundler MR, Singhal S, Cowan MA, Rabosky DL. Is genomic diversity a useful proxy for census population size? Evidence from a species‐rich community of desert lizards. Mol Ecol. 2019;28:1664–1674. doi: 10.1111/mec.15042 30739375


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2019 Číslo 12