期刊论文详细信息
BMC Evolutionary Biology
Molecular species delimitation of a symbiotic fig-pollinating wasp species complex reveals extreme deviation from reciprocal partner specificity
James M Cook2  Sarah al-Beidh3  Clive T Darwell1 
[1] Department of Biology, Syracuse University, 107 College Place, Syracuse 13244, NY, USA;Hawkesbury Institute for the Environment, University of Western Sydney, Locked Bag 1797, Penrith South DC 1797, NSW, Australia;Royal Horticultural Society, Wisley Garden, Woking, Surrey GU23 6QB, UK
关键词: Wasp;    Pollinator;    Ficus;    Agaonidae;    Species delimitation;   
Others  :  1117944
DOI  :  10.1186/s12862-014-0189-9
 received in 2014-05-22, accepted in 2014-08-13,  发布年份 2014
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【 摘 要 】

Background

Symbiotic relationships have contributed to major evolutionary innovations, the maintenance of fundamental ecosystem functions, and the generation and maintenance of biodiversity. However, the exact nature of host/symbiont associations, which has important consequences for their dynamics, is often poorly known due to limited understanding of symbiont taxonomy and species diversity. Among classical symbioses, figs and their pollinating wasps constitute a highly diverse keystone resource in tropical forest and savannah environments. Historically, they were considered to exemplify extreme reciprocal partner specificity (one-to-one host-symbiont species relationships), but recent work has revealed several more complex cases. However, there is a striking lack of studies with the specific aims of assessing symbiont diversity and how this varies across the geographic range of the host.

Results

Here, we use molecular methods to investigate cryptic diversity in the pollinating wasps of a widespread Australian fig species. Standard barcoding genes and methods were not conclusive, but incorporation of phylogenetic analyses and a recently developed nuclear barcoding gene (ITS2), gave strong support for five pollinator species. Each pollinator species was most common in a different geographic region, emphasising the importance of wide geographic sampling to uncover diversity, and the scope for divergence in coevolutionary trajectories across the host plant range. In addition, most regions had multiple coexisting pollinators, raising the question of how they coexist in apparently similar or identical resource niches.

Conclusion

Our study offers a striking example of extreme deviation from reciprocal partner specificity over the full geographical range of a fig-wasp system. It also suggests that superficially identical species may be able to co-exist in a mutualistic setting albeit at different frequencies in relation to their fig host’s range. We show that comprehensive sampling and molecular taxonomic techniques may be required to uncover the true structure of cryptic biodiversity underpinning intimate ecological interactions.

【 授权许可】

   
2014 Darwell et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Margulis L: Origin of Eukaryotic Cells. Yale University Press, Newhaven, Connecticut; 1970.
  • [2]Kiers ET, Rousseau RA, West SA, Denison RF: Host sanctions and the legume–rhizobium mutualism. Nature 2003, 425:78-81.
  • [3]Darwin C: On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. John Murray, London, UK; 1859.
  • [4]Leigh EG: The evolution of mutualism. J Evol Biol 2010, 23(12):2507-2528.
  • [5]Althoff DM, Segraves KA, Johnson MTJ: Testing for coevolutionary diversification: linking pattern with process. Trends Ecol Evol 2014, 29(2):82-89.
  • [6]Thrall PH, Hochberg ME, Burdon JJ, Bever JD: Coevolution of symbiotic mutualists and parasites in a community context. Trends Ecol Evol 2007, 22(3):120-126.
  • [7]Rooney N, McCann KS: Integrating food web diversity, structure and stability. Trends Ecol Evol 2012, 27(1):40-46.
  • [8]Herre EA, Knowlton N, Mueller UG, Rehner SA: The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 1999, 14(2):49-53.
  • [9]Cook JM, Rasplus JY: Mutualists with attitude: coevolving fig wasps and figs. Trends Ecol Evol 2003, 18(7):241-248.
  • [10]Herre EA, Jander KC, Machado CA: Evolutionary ecology of figs and their associates: recent progress and outstanding puzzles. Annu Rev Ecol Evol Syst 2008, 39:439-458.
  • [11]Segar ST, Cook JM: The dominant exploiters of the fig/pollinator mutualism vary across continents, but their costs fall consistently on the male reproductive function of figs. Ecol Entomol 2012, 37:342-349.
  • [12]Kissling WD, Rahbek C, Bohning-Gaese K: Food plant diversity as broad-scale determinant of avian frugivore richness. Proc R Soc B-Biol Sci 2007, 274(1611):799-808.
  • [13]Lopez-Vaamonde C, Rasplus JY, Weiblen GD, Cook JM: Molecular phylogenies of fig wasps: partial cocladogenesis of pollinators and parasites. Mol Phylogenet Evol 2001, 21(1):55-71.
  • [14]Weiblen GD: How to be a fig wasp. Annu Rev Entomol 2002, 47:299-330.
  • [15]Molbo D, Machado CA, Sevenster JG, Keller L, Herre EA: Cryptic species of fig-pollinating wasps: implications for the evolution of the fig-wasp mutualism, sex allocation, and precision of adaptation. Proc Natl Acad Sci U S A 2003, 100(10):5867-5872.
  • [16]Molbo D, Machado CA, Herre EA, Keller L: Inbreeding and population structure in two pairs of cryptic fig wasp species. Mol Ecol 2004, 13(6):1613-1623.
  • [17]Haine ER, Martin J, Cook JM: Deep mtDNA divergences indicate cryptic species in a fig-pollinating wasp. BMC Evol Biol 2006, 6:83. BioMed Central Full Text
  • [18]Chen Y, Compton SG, Liu M, Chen X-Y: Fig trees at the northern limit of their range: the distributions of cryptic pollinators indicate multiple glacial refugia. Mol Ecol 2012, 21(7):1687-1701.
  • [19]Cornille A, Underhill JG, Cruaud A, Hossaert-McKey M, Johnson SD, Tolley KA, Kjellberg F, van Noort S, Proffit M: Floral volatiles, pollinator sharing and diversification in the fig-wasp mutualism: insights from Ficus natalensis, and its two wasp pollinators (South Africa). Proc Roy Soc B: Biol Sci 2012, 279:1731-1739.
  • [20]McLeish MJ, van Noort S: Codivergence and multiple host species use by fig wasp populations of the Ficus pollination mutualism.BMC Evol Biol, 12:1–2012.
  • [21]Compton SG, Grehan K, van Noort S: A fig crop pollinated by three or more species of agaonid fig wasps. African Entomol 2009, 17(2):215-222.
  • [22]Machado CA, Robbins N, Gilbert MTP, Herre EA: Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proc Natl Acad Sci U S A 2005, 102:6558-6565.
  • [23]Cook JM, Segar ST: Speciation in fig wasps. Ecol Entomol 2010, 35:54-66.
  • [24]Kobmoo N, Hossaert-Mckey M, Rasplus JY, Kjellberg F: Ficus racemosa is pollinated by a single population of a single agaonid wasp species in continental South-East Asia. Mol Ecol 2010, 19:2700-2712.
  • [25]Kaartinen R, Stone GN, Hearn J, Lohse K, Roslin T: Revealing secret liaisons: DNA barcoding changes our understanding of food webs. Ecol Entomol 2010, 35(5):623-638.
  • [26]Smith MA, Eveleigh ES, McCann KS, Merilo MT, McCarthy PC, Van Rooyen KI: Barcoding a quantified food web: crypsis, concepts, ecology and hypotheses. PLoS One 2011, 6(7):e14424.
  • [27]Wheeler QD, Raven PH, Wilson EO: Taxonomy: impediment or expedient? Sci (New York, NY) 2004, 303(5656):285.
  • [28]Cook JM, West SA: Figs and fig wasps. Curr Biol 2005, 15(24):R978-R980.
  • [29]Lopez-Vaamonde C, Dixon DJ, Cook JM, Rasplus JY: Revision of the Australian species of pleistodontes (Hymenoptera : Agaonidae) fig-pollinating wasps and their host-plant associations. Zool J Linn Soc 2002, 136(4):637-683.
  • [30]Vogler AP, Monaghan MT: Recent advances in DNA taxonomy. J Zool Syst Evol Res 2007, 45(1):1-10.
  • [31]Moritz C, Cicero C: DNA barcoding: promise and pitfalls. Plos Biol 2004, 2(10):1529-1531.
  • [32]Will KW, Rubinoff D: Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics- Int J Willi Hennig Soc 2004, 20(1):47-55.
  • [33]Hebert PDN, Ratnasingham S, deWaard JR: “Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species,”. Proc R Soc London Ser B-Biological Sci 2003, 270:S96-S99.
  • [34]Hebert PDN, Cywinska A, Ball SL, DeWaard JR: Biological identifications through DNA barcodes. Proc R Soc London Ser B-Biological Sci 2003, 270(1512):313-321.
  • [35]Cruaud A, Jabbour-Zahab R, Genson G, Couloux A, Peng Y-Q, Da Rong Y, Ubaidillah R, Santinelo Pereira RA, Kjellberg F, van Noort S, Kerdelhue C, Rasplus J-Y: Out of Australia and back again: the world-wide historical biogeography of non-pollinating fig wasps (Hymenoptera: Sycophaginae). J Biogeogr 2011, 38(2):209-225.
  • [36]Lopez-Vaamonde C, Wikstrom N, Kjer KM, Weiblen GD, Rasplus JY, Machado CA, Cook JM: Molecular dating and biogeography of fig-pollinating wasps. Mol Phylogenet Evol 2009, 52(3):715-726.
  • [37]Avise J: Phylogeography: The History And Formation Of Species. Harvard University Press, Cambridge Massachusetts, London England; 2000.
  • [38]Wiemers M, Fiedler K: Does the DNA barcoding gap exist? - a case study in blue butterflies (Lepidoptera: Lycaenidae). Front Zool 2007, 4:8. BioMed Central Full Text
  • [39]Hurst GDD, Jiggins FM: Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc R Soc B-Biol Sci 2005, 272(1572):1525-1534.
  • [40]Lohse K, Sharanowski B, Blaxter M, Nicholls JA, Stone GN: Developing EPIC markers for chalcidoid Hymenoptera from EST and genomic data. Mol Ecol Resour 2011, 11(3):521-529.
  • [41]Coleman AW: Is there a molecular key to the level of ‘biological species’ in eukaryotes? A DNA guide. Mol Phylogenet Evol 2009, 50(1):197-203.
  • [42]Li YW, Zhou X, Feng G, Hu HY, Niu LM, Hebert PDN, Huang DW: COI and ITS2 sequences delimit species, reveal cryptic taxa and host specificity of fig-associated Sycophila (Hymenoptera, Eurytomidae). Mol Ecol Resour 2010, 10(1):31-40.
  • [43]Muller T, Philippi N, Dandekar T, Schultz J, Wolf M: Distinguishing species. Rna-a Publ Rna Soc 2007, 13(9):1469-1472.
  • [44]Zhou MJ, Xiao JH, Bian SN, Li YW, Niu LM, Hu HY, Wu WS, Murphy RW, Huang DW: Molecular approaches identify known species, reveal cryptic species and verify host specificity of Chinese Philotrypesis (Hymenoptera: Pteromalidae). Mol Ecol Resour 2012, 12(4):598-606.
  • [45]Eldredge N, Cracraft J: Phylogenetic Patterns And The Evolutionary Process Method And Theory In Comparative Biology. In Phylogenetic Patterns and the Evolutionary Process: Method and Theory in Comparative Biology. Viii+349p. Edited by Eldredge N, Cracraft J. Columbia University Press, New York, N.Y., USA. Illus. Maps; 1980.
  • [46]Dixon DJ, Jackes BR, Bielig LM: Figuring out the figs: the ficus obliqua-ficus rubiginosa complex (Moraceae : Urostigma sect. Malvanthera). Aust Syst Bot 2001, 14(1):133-154.
  • [47]Lopez-Vaamonde C, Dixon DJ, Cook JM, Rasplus JY: Revision of the Australian species of pleistodontes (Hymenoptera : Agaonidae) fig-pollinating wasps and their host-plant associations. Zool J Linn Soc 2002, 136(4):637-683.
  • [48]De Queiroz K: Species concepts and species delimitation. Syst Biol 2007, 56(6):879-886.
  • [49]Moe AM, Weiblen GD: Molecular divergence in allopatric ceratosolen (Agaonidae) pollinators of geographically widespread ficus (Moraceae) species. Ann Entomol Soc Am 2010, 103(6):1025-1037.
  • [50]Bruno JF, Cardinale BJ: Cascading effects of predator richness. Front Ecol Environ 2008, 6(10):539-546.
  • [51]Lowe Harris A, S Ashton P: Ecological Genetics. Blackwell Science limited, Carlton, Victoria, Australia; 2004.
  • [52]Thompson JN: The Geographic Mosaic of Coevolution. The University of Chicago Press, Chicago; 2005.
  • [53]Zhang DY, Lin K, Hanski I: Coexistence of cryptic species. Ecol Lett 2004, 7(3):165-169.
  • [54]Weiblen GD, Bush GL: Speciation in fig pollinators and parasites. Mol Ecol 2002, 11(8):1573-1578.
  • [55]Compton SG, Holton KC, Rashbrook VK, Vannoort S, Vincent SL, Ware AB: Studies of Ceratosolen galili, a non-pollinating agaonid fig wasp. Biotropica 1991, 23(2):188-194.
  • [56]Peng Y-Q, Duan Z-B, Yang D-R, Rasplus J-Y: Co-occurrence of two Eupristina species on Ficus altissima in Xishuangbanna, SW China. Symbiosis 2008, 45(1–3):9-14.
  • [57]Warren M, Robertson MP, Greeff JM: A comparative approach to understanding factors limiting abundance patterns and distributions in a fig tree-fig wasp mutualism. Ecography (Cop) 2010, 33(1):148-158.
  • [58]West SA, Cook JM, Werren JH, Godfray HCJ: Wolbachia in two insect host-parasitoid communities. Mol Ecol 1998, 7(11):1457-1465.
  • [59]Xiao J-H, Wang N-X, Li Y-W, Murphy RW, Wan D-G, Niu L-M, Hu H-Y, Fu Y-G, Huang D-W: Molecular approaches to identify cryptic species and polymorphic species within a complex community of fig wasps. PLoS One 2010, 5(11):e15067.
  • [60]Jermiin LS, Crozier RH: The cytochrome-B region in the mitochondrial DNA of the ant Tetraponera rufoniger - sequence divergence in hymenoptera may be associated with nucleotide content. J Mol Evol 1994, 38(3):282-294.
  • [61]White T, Bruns T, Lee S, Taylor J: Amplification And Direct Sequencing Of Fungal Ribosomal Genes For Phylogenies. Academic, New York, N.Y.; 1990.
  • [62]Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P: Evolution, weighting, and phylogenetic utility of mitochondrial gene-sequences and a compilation of conserved polymerase chain-reaction primers. Ann Entomol Soc Am 1994, 87(6):651-701.
  • [63]Hall TA: BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows95/98NT. Nucleic Acids Symp 1999, 41:95-98.
  • [64]Harris DJ, Crandall KA: Intragenomic variation within ITS1 and ITS2 of freshwater crayfishes (Decapoda: Cambaridae): implications for phylogenetic and microsatellite studies. Mol Biol Evol 2000, 17:284-291.
  • [65]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19(12):1572-1574.
  • [66]Darriba D, Taboada GL, Doallo R, Posada D: jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012, 9(8):772.
  • [67]Swofford DL: PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland, Massachusetts, USA; 2002.
  • [68]Jones M, Ghoorah A, Blaxter M: jMOTU and taxonerator: turning DNA barcode sequences into annotated operational taxonomic units. PLoS One 2011, 6(4):10.
  • [69]Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP: Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 2006, 55(4):595-609.
  • [70]Ezard T, Fujisawa T, Barraclough T: Species’ Limits by Threshold Statistics. 2009.
  • [71]R: A language and environment for statistical computing R Found Stat Comput 2011, 1:409.
  • [72]Drummond AJ, Rambaut A: BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007, 7:214. BioMed Central Full Text
  • [73]Baele G, Lemey P, Rambaut A, Suchard MA, Alekseyenko AV: Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty.Mol Biol Evol 2012, In press.
  • [74]Raftery AE: Hypothesis testing and model selection. In Markov chain Monte Carlo in practice. Edited by Gilks WR, Richardson S, Spiegelhalter DJ. Chapman & Hall, London; 1996.
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