Geographic parthenogenesis and plant-enemy interactions in the common dandelion

BMC Evolutionary Biology

Arjen Biere¹  Koen JF Verhoeven¹ 

[1] Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, Wageningen, 6708 PB, The Netherlands

关键词: Soil feedback;    Plant-pathogen interactions;    Plant-insect interactions;    Taraxacum;    Red Queen;   

Others  :  1130094
DOI  :  10.1186/1471-2148-13-23

 received in 2012-06-26, accepted in 2013-01-16,  发布年份 2013

【 摘 要 】

Background

Many species with sexual and asexual variants show a pattern of geographic parthenogenesis where asexuals have broader and higher-latitude distribution than sexuals. Because sexual reproduction is often considered a costly evolutionary strategy that is advantageous in the face of selection by coevolving pests and pathogens, one possible explanation for geographic parthenogenesis is that populations at higher latitudes are exposed to fewer pests and pathogens. We tested this hypothesis in the common dandelion (Taraxacum officinale), a species with well-established geographic parthenogenesis, by screening prevalence and effects of several specialized pests and pathogens in natural dandelion populations.

Results

We did a population survey of 18 dandelion populations along a geographic transect that ranged from the area where sexual and asexual dandelions co-occur northward into the area where only asexuals occur. In addition we used four southern and four northern populations in a 8x8 cross-inoculation greenhouse experiment in which plants were exposed experimentally to each other’s natural field soil microbial communities. The cross-inoculation experiment indicated a higher pathogenicity of soil microbial communities from the southern, mostly sexual, populations compared to soil microbial communities from the northern asexual populations. Northern dandelion populations also showed reduced infestation by a specialized seed-eating weevil. A similar trend of reduced rust fungus infection in northern populations was observed but this trend was not statistically significant.

Conclusions

The prevalence of pests and pathogens decreased along the south-to-north axis of geographic parthenogenesis. This highlights the potential of biotic interactions in shaping patterns of geographic parthenogenesis.

【 授权许可】

   
2013 Verhoeven and Biere; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Bierzychudek P: Patterns in plant parthenogenesis. Experientia 1985, 41(10):1255-1264.
• [2]Buckley TR, Marske K, Attanayake D: Phylogeography and ecological niche modelling of the New Zealand stick insect Clitarchus hookeri (White) support survival in multiple coastal refugia. J Biogeogr 2010, 37(4):682-695.
• [3]Law JH, Crespi BJ: The evolution of geographic parthenogenesis in Timema walking-sticks. Mol Ecol 2002, 11(8):1471-1489.
• [4]Martins MJF, Vandekerkhove J, Namiotko T: Environmental stability and the distribution of the sexes: insights from life history experiments with the geographic parthenogen Eucypris virens (Crustacea: Ostracoda). Oikos 2008, 117(6):829-836.
• [5]Thompson SL, Whitton J: Patterns of recurrent evolution and geographic parthenogenesis within apomictic polyploid Easter daises (Townsendia hookeri). Mol Ecol 2006, 15(11):3389-3400.
• [6]Adolfsson S, Michalakis Y, Paczesniak D, Bode SNS, Butlin RK, Lamatsch DK, Martins MJF, Schmit O, Vandekerkhove J, Jokela J: Evaluation of elevated ploidy and asexual reproduction as alternative explanations for geographic parthenogenesis in Eucypris virens ostracods. Evolution 2010, 64(4):986-997.
• [7]Britton NF, Mogie M: Poor male function favours the coexistence of sexual and asexual relatives. Ecol Lett 2001, 4(2):116-121.
• [8]Haag CR, Ebert D: A new hypothesis to explain geographic parthenogenesis. Annales Zoologici Fennici 2004, 41(4):539-544.
• [9]Kearney M: Hybridization, glaciation and geographical parthenogenesis. Trends Ecol Evol 2005, 20(9):495-502.
• [10]Horandl E: The complex causality of geographical parthenogenesis. New Phytol 2006, 171(3):525-538.
• [11]Lynch M: Destabilizing hybridization, general purpose genotypes and geographic parthenogenesis. Q Rev Biol 1984, 59(3):257-290.
• [12]Stebbins GL: Variation and evolution in plants. New York: Columbia University Press; 1950.
• [13]Bell G: The masterpiece of nature: the evolution and genetics of sexuality. Berkeley: California Press; 1982.
• [14]Glesener RR, Tilman D: Sexuality and components of environmental uncertainty: clues from geographic parthenogenesis in terrestrial animals. Amer Nat 1978, 112(986):659-673.
• [15]Jeanike J: An hypothesis to account for the maintenance of the sex within populations. Evol Theory 1978, 3:191-194.
• [16]Hamilton WD: Sex versus non-sex versus parasite. Oikos 1980, 35:282-290.
• [17]Decaestecker E, Gaba S, Raeymaekers JAM, Stoks R, Van Kerckhoven L, Ebert D, De Meester L: Host-parasite ‘Red Queen’ dynamics archived in pond sediment. Nature 2007, 450(7171):870-874.
• [18]Dybdahl MF, Lively CM: Host-parasite coevolution: Evidence for rare advantage and time-lagged selection in a natural population. Evolution 1998, 52(4):1057-1066.
• [19]Kerstes NAG, Berenos C, Schmid-Hempel P, Wegner KM: Antagonistic experimental coevolution with a parasite increases host recombination frequency. Bmc Evol Bio 2012, 12:18. BioMed Central Full Text
• [20]Morran LT, Schmidt OG, Gelarden IA, Parrish RC, Lively CM: Running with the Red Queen: Host-parasite coevolution selects for biparental sex. Science 2011, 333(6039):216-218.
• [21]Lively CM: A review of Red Queen models for the persistence of obligate sexual reproduction. J Hered 2010, 101:S13-S20.
• [22]Hartfield M, Keightley PD: Current hypotheses for the evolution of sex and recombination. Integrative Zoology 2012, 7(2):192-209.
• [23]Coley PD, Barone JA: Herbivory and plant defenses in tropical forests. Ann Rev Ecol Evol Syst 1996, 27:305-335.
• [24]Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K: Is there a latitudinal gradient in the importance of biotic interactions? Ann Rev Ecol Evol Syst 2009, 40:245-269.
• [25]Coley PD, Aide TM: Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests. In Plant-animal interactions: Evolutionary ecology in tropical and temperate regions. Edited by Price PW, Lewinsohn TM, Fernandes GW, Benson WW. New York: Wiley; 1991:25-49.
• [26]Moles AT, Bonser SP, Poore AGB, Wallis IR, Foley WJ: Assessing the evidence for latitudinal gradients in plant defence and herbivory. Funct Ecol 2011, 25(2):380-388.
• [27]Moles AT, Wallis IR, Foley WJ, Warton DI, Stegen JC, Bisigato AJ, Cella-Pizarro L, Clark CJ, Cohen PS, Cornwell WK, et al.: Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes. New Phytol 2011, 191(3):777-788.
• [28]Johnson MTJ, Rasmann S: The latitudinal herbivory-defence hypothesis takes a detour on the map. New Phytol 2011, 191(3):589-592.
• [29]Springer YP: Edaphic quality and plant-pathogen interactions: effects of soil calcium on fungal infection of a serpentine flax. Ecol 2009, 90(7):1852-1862.
• [30]Albrectsen BR, Witzell J, Robinson KM, Wulff S, Luquez VMC, Agren R, Jansson S: Large scale geographic clines of parasite damage to Populus tremula L. Ecography 2010, 33(3):483-493.
• [31]Burdon JJ, Oates JD, Marshall DR: Interactions between Avena and Puccinia species. 1. The wild hosts: Avena barbata Pott Ex Link, A. fatua L., A. ludoviciana Durieu. J Appl Ecol 1983, 20(2):571-584.
• [32]Seabloom EW, Borer ET, Mitchell CE, Power AG: Viral diversity and prevalence gradients in North American Pacific Coast grasslands. Ecology 2010, 91(3):721-732.
• [33]Chu HY, Fierer N, Lauber CL, Caporaso JG, Knight R, Grogan P: Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol 2010, 12(11):2998-3006.
• [34]Johnson MTJ, Smith SD, Rausher MD: Effects of plant sex on range distributions and allocation to reproduction. New Phytol 2010, 186(3):769-779.
• [35]Silvertown J: The evolutionary maintenance of sexual reproduction: Evidence from the ecological distribution of asexual reproduction in clonal plants. Int J Plant Sci 2008, 169(1):157-168.
• [36]Johnson MTJ, Smith SD, Rausher MD: Plant sex and the evolution of plant defenses against herbivores. Proc Natl Acad Sci USA 2009, 106(43):18079-18084.
• [37]Menken SBJ, Smit E, DenNijs HCM: Genetical population structure in plants: Gene flow between diploid sexual and triploid asexual dandelions (Taraxacum section Ruderalia). Evolution 1995, 49(6):1108-1118.
• [38]Mogie M, Ford H: Sexual and asexual Taraxacum species. Biol J Linn Soc 1988, 35(2):155-168.
• [39]van Dijk PJ: Ecological and evolutionary opportunities of apomixis: insights from Taraxacum and Chondrilla. Philos Trans R Soc Lond B Biol Sci 2003, 358(1434):1113-1120.
• [40]Kulmatiski A, Beard KH, Stevens JR, Cobbold SM: Plant-soil feedbacks: a meta-analytical review. Ecol Lett 2008, 11(9):980-992.
• [41]Lively CM: Trematode infection and the distribution and dynamics of parthenogenetic snail populations. Parasitology 2001, 123:S19-S26.
• [42]Lively CM: Parthenogenesis in a fresh-water snail: reproductive assurance versus parasitic release. Evolution 1992, 46(4):907-913.
• [43]Lively CM: Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature 1987, 328(6130):519-521.
• [44]Ben-Ami F, Heller J: Spatial and temporal patterns of parthenogenesis and parasitism in the freshwater snail Melanoides tuberculata. J Evol Biol 2005, 18(1):138-146.
• [45]Killick SC, Obbard DJ, West SA, Little TJ: Parasitism and breeding system variation in North American populations of Daphnia pulex. Ecol Res 2008, 23(1):235-240.
• [46]Rasmann S, Agrawal AA: Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecol Lett 2011, 14(5):476-483.
• [47]Kumpulainen T, Grapputo A, Mappes J: Parasites and sexual reproduction in psychid moths. Evolution 2004, 58(7):1511-1520.
• [48]Meirmans S, Skorping A, Loyning MK, Kirkendall LR: On the track of the Red Queen: bark beetles, their nematodes, local climate and geographic parthenogenesis. J Evol Biol 2006, 19(6):1939-1947.
• [49]van der Hulst RGM, Mes THM, den Nijs JCM, Bachmann K: Amplified fragment length polymorphism (AFLP) markers reveal that population structure of triploid dandelions (Taraxacum officinale) exhibits both clonality and recombination. Mol Ecol 2000, 9(1):1-8.
• [50]Lively CM, Howard RS: Selection by parasites for clonal diversity and mixed mating. Philos Trans R Soc Lond B Biol Sci 1994, 346(1317):271-280.
• [51]Burdon JJ, Groves RH, Cullen JM: The impact of biological control on the distribution and abundance of Chondrilla juncea in Western Australia. J Appl Ecol 1981, 18(3):957-966.
• [52]Roy BA, Bierzychudek P: The potential for rust infection to cause natural selection in apomictic Arabis holboelli (Brassicaceae). Oecologia 1993, 95(4):533-541.
• [53]Chaboudez P, Burdon JJ: Frequency-dependent selection in a wild plant-pathogen system. Oecologia 1995, 102(4):490-493.
• [54]Siemens DH, Roy BA: Tests for parasite-mediated frequency-dependent selection in natural populations of an asexual plant species. Evol Ecol 2005, 19(4):321-338.
• [55]Honek A, Martinkova Z: Pre-dispersal predation of Taraxacum officinale (dandelion) seed. J Ecol 2005, 93(2):335-344.
• [56]Dobes C, Mitchell-Olds T, Koch MA: Intraspecific diversification in North American Boechera stricta (=Arabis drummondii), Boechera x divaricarpa, and Boechera holboellii (Brassicaceae) inferred from nuclear and chloroplast molecular markers - an integrative approach. Am J Bot 2004, 91(12):2087-2101.
• [57]Brinkman EP, Van der Putten WH, Bakker EJ, Verhoeven KJF: Plant-soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 2010, 98(5):1063-1073.
• [58]Bever JD: Feedback between plants and their soil communities in an old field community. Ecology 1994, 75(7):1965-1977.
• [59]Kardol P, Bezemer TM, van der Putten WH: Temporal variation in plant-soil feedback controls succession. Ecol Lett 2006, 9(9):1080-1088.
• [60]Van der Putten WH, Van Dijk C, Peters BAM: Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 1993, 362(6415):53-56.
• [61]Klironomos JN: Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 2002, 417(6884):67-70.
• [62]Felker-Quinn E, Bailey JK, Schweitzer JA: Soil biota drive expression of genetic variation and development of population-specific feedbacks in an invasive plant. Ecology 2011, 92(6):1208-1214.
• [63]Dodds P, Thrall P: Recognition events and host-pathogen co-evolution in gene-for-gene resistance to flax rust. Funct Plant Biol 2009, 36(5):395-408.
• [64]Clay K, Kover PX: The Red Queen Hypothesis and plant/pathogen interactions. Annu Rev Phytopathol 1996, 34:29-50.
• [65]Otto SP, Nuismer SL: Species interactions and the evolution of sex. Science 2004, 304(5673):1018-1020.
• [66]Agrawal A, Lively CM: Infection genetics: gene-for-gene versus matching-alleles models and all points in between. Evol Ecol Res 2002, 4(1):79-90.
• [67]Waters CW: The control of teliospore and urediniospore formation by experimental methods. Phytopathol 1928, 18:157-213.
• [68]Termorshuizen AJ, Swertz CA: Dutch rust fungi. Doorwerth: Termorshuizen; 2011.
• [69]Gumovsky AV: Parasitism of Entedon costalis (Hymenoptera: Eulophidae) in Glocianus punctiger (Coleoptera: Curculionidae): an example of intentional discovery of the parasitoid-host association. Zootaxa 1964, 2008:40-68.
• [70]Tas ICQ, Van Dijk PJ: Crosses between sexual and apomictic dandelions (Taraxacum). I. The inheritance of apomixis. Heredity 1999, 83:707-714.