Oecologia

, Volume 186, Issue 2, pp 471–482 | Cite as

Reproductive ecology of a parasitic plant differs by host species: vector interactions and the maintenance of host races

Population ecology – original research

Abstract

Parasitic plants often attack multiple host species with unique defenses, physiology, and ecology. Reproductive phenology and vectors of parasitic plant genes (pollinators and dispersers) can contribute to or erode reproductive isolation of populations infecting different host species. We asked whether desert mistletoe, Phoradendron californicum (Santalaceae tribe Visceae syn. Viscaceae), differs ecologically across its dominant leguminous hosts in ways affecting reproductive isolation. Parasite flowering phenology on one host species (velvet mesquite, Prosopis velutina) differed significantly from that on four others, and phenology was not predicted by host species phenology or host individual. Comparing mistletoe populations on mesquite and another common host species (catclaw acacia, Senegalia greggii) for which genetically distinct host races are known, we tested for differences in interactions with vectors by quantifying pollinator visitation, reward production, pollen receipt, and fruit consumption. Mistletoes on mesquite produced more pollinator rewards per flower (1.86 times the nectar and 1.92 times the pollen) and received ~ 2 more pollen grains per flower than those on acacia. Mistletoes on the two host species interacted with distinct but overlapping pollinator communities, and pollinator taxa differed in visitation according to host species. Yet, mistletoes of neither host showed uniformly greater reproductive success. Fruit set (0.70) did not differ by host, and the rates of fruit ripening and removal differed in contrasting ways. Altogether, we estimate strong but asymmetric pre-zygotic isolating barriers between mistletoes on the two hosts. These host-associated differences in reproduction have implications for interactions with mutualist vectors and population genetic structure.

Keywords

Phenology Pollination Mistletoe Reproductive isolation Seed dispersal 

Notes

Acknowledgements

We thank J. Knighton/Wisor, M. A. Iacuelli, A. L. Pond, E. May, and J. P. Berry for help with fieldwork and the Bronstein lab group for helpful comments. We acknowledge support from the following: a National Science Foundation (NSF) Doctoral Dissertation Improvement Grant to KMY and JLB (DEB-1601370), a Graduate Research Fellowship to KMY (DGE-1143953), a Ginny Saylor Research Grant from the Arizona Native Plants Society to KMY, and a University of Arizona Graduate Research and Project Grant to KMY.

Author contribution statement

KMY and JLB conceived the study. KMY conducted the field work and data analyses. KMY and JLB wrote the manuscript.

Supplementary material

442_2017_4038_MOESM1_ESM.docx (10.4 mb)
Supplementary material 1 (DOCX 10660 kb)
442_2017_4038_MOESM2_ESM.docx (33 mb)
Supplementary material 2 (DOCX 33752 kb)
442_2017_4038_MOESM3_ESM.docx (41 kb)
Supplementary material 3 (DOCX 40 kb)
442_2017_4038_MOESM4_ESM.docx (5.6 mb)
Supplementary material 4 (DOCX 5711 kb)
442_2017_4038_MOESM5_ESM.docx (28 kb)
Supplementary material 5 (DOCX 28 kb)

References

  1. Altizer SM, Thrall PH, Antonovics J (1998) Vector behavior and the transmission of anther-smut infection in Silene alba. Am Midl Nat 139:147–163. https://doi.org/10.1674/0003-0031(1998)139[0147:vbatto]2.0.co;2Google Scholar
  2. Aukema JE (2002) Variation in mistletoe seed deposition: effects of intra- and interspecific host characteristics. Ecography 25:139–144CrossRefGoogle Scholar
  3. Aukema JE (2003) Vectors, viscin, and Viscaceae: mistletoes as parasites, mutualists, and resources. Front Ecol Environ 1:212–219CrossRefGoogle Scholar
  4. Aukema JE (2004) Distribution and dispersal of desert mistletoe is scale-dependent, hierarchically nested. Ecography 27:137–144CrossRefGoogle Scholar
  5. Brody AK (1997) Effects of pollinators, herbivores, and seed predators on flowering phenology. Ecology 78:1624–1631CrossRefGoogle Scholar
  6. Burgess TL (1995) Desert grassland, mixed shrub savanna, shrub steppe, or semidesert scrub? The dilemma of coexisting growth forms. In: McClaran MP, Van Devender TR (eds) The desert grassland. Univ. of Arizona Press, USA, pp 31–64Google Scholar
  7. Calero-Torralbo M, Valera (2008) Synchronization of host-parasite cycles by means of diapause: Host influence and parasite response to involuntary host shifting. Parasitol 135:1343–1352CrossRefGoogle Scholar
  8. Candia AB, Medel R, Fonturbel FE (2014) Indirect positive effects of a parasitic plant on host pollination and seed dispersal. Oikos 123:1371–1376CrossRefGoogle Scholar
  9. Caraballo-Ortiz MA, Gonzalez-Castro A, Yang S, dePamphilis CW, Carlo TA (2017) Dissecting the contributions of dispersal and host properties to the local abundance of a tropical mistletoe. J Ecol 105:1657–1667CrossRefGoogle Scholar
  10. Clark RM, Thompson R (2011) Estimation and comparison of flowering curves. Plant Ecol Divers 4:189–200.  https://doi.org/10.1080/17550874.2011.580382 CrossRefGoogle Scholar
  11. Clay K, Dement D, Rejmanek M (1985) Experimental evidence for host races in Mistletoe (Phoradendron tomentosum). Am J Bot 72:1225–1231CrossRefGoogle Scholar
  12. Craig TP, Horner JD, Itami JK (1997) Hybridization studies on the host races of Eurosta solidaginis: implications for sympatric speciation. Evol 51:1552–1560.  https://doi.org/10.1111/j.1558-5646.1997.tb01478.x Google Scholar
  13. De Vega C, Berjano R, Arista M, Ortiz PL, Talavera S, Stuessy TF (2008) Genetic races associated with the genera and sections of host species in the holoparasitic plant Cytinus (Cytinaceae) in the Western Mediterranean basin. New Phytol 178:875–887.  https://doi.org/10.1111/j.1469-8137.2008.02423.x CrossRefPubMedGoogle Scholar
  14. De Vienne DM, Refrégier G, López-Villavicencio M, Tellier A, Hood ME, Giraud T (2013) Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. New Phytol 198:347–385.  https://doi.org/10.1111/nph.12150 CrossRefPubMedGoogle Scholar
  15. Drès M, Mallet J (2002) Host races in plant-feeding insects and their importance in sympatric speciation. Philos Trans R Soc Lond B Biol Sci 357:471–492.  https://doi.org/10.1098/rstb.2002.1059 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Feder JL, Filchak KE (1999) It’s about time: The evidence for host plant-mediated selection in the apple maggot fly, Rhagoletis pomonella, and its implications for fitness trade-offs in phytophagous insects. Entomol Exp Appl 91:211–225.  https://doi.org/10.1023/A:1003603918154 CrossRefGoogle Scholar
  17. Ferrari J, Godfray HCJ, Faulconbridge AS, Prior K, Via S (2006) Population differentiation and genetic variation in host choice among pea aphid from eight host plant genera. Evolution 60:1574–1584CrossRefPubMedGoogle Scholar
  18. Gaddis KD (2014) The population biology of dispersal and gene flow in the desert shrub Acacia (Senegalia) greggii A. Gray in the Mojave National Preserve. In: Ph.D. thesis, University of California, Los Angeles, CAGoogle Scholar
  19. Gibson CC, Watkinson AR (1989) The host range and selectivity of a parasitic plant: Rhinanthus minor L. Oecologia 78:401–406CrossRefPubMedGoogle Scholar
  20. Glazner JT, Devhn B, Ellstrand NC (1988) Biochemical and morphological evidence for host race evolution in desert mistletoe, Phoradendron californicum (Viscaceae). Plant Syst Evol 161:13–21CrossRefGoogle Scholar
  21. Hopkins R (2013) Reinforcement in plants. New Phytol 197:1095–1103.  https://doi.org/10.1111/nph.12119 CrossRefPubMedGoogle Scholar
  22. Jerome CA, Ford BA (2002) The discovery of three genetic races of the dwarf mistletoe Arceuthobium americanum (Viscaceae) provides insight into the evolution of parasitic angiosperms. Mol Ecol 11:387–405CrossRefPubMedGoogle Scholar
  23. Kahle-Zuber D (2008) Biology and evolution of the European mistletoe (Viscum album). In: Ph.D thesis, ETH Zurich, Zurich, SwitzerlandGoogle Scholar
  24. Kelly D, Ladley JJ, Robertson AW (2007) Is the pollen-limited mistletoe Peraxilla tetrapetala (Loranthaceae) also seed limited? Aust Ecol 32:850–857CrossRefGoogle Scholar
  25. Keys R, Buchmann S, Smith S (1995) Pollination effectiveness and pollination efficiency of insects foraging Prosopis velutina in south-eastern Arizona. J Appl Ecol 32:519–527.  https://doi.org/10.2307/2404649 CrossRefGoogle Scholar
  26. Kiss L, Pintye A, Kovacs GM, Jankovics T, Fontaine MC, Harvey N, Xu X, Nicot PC, Bardin M, Shykoff JA, Giraud T (2011) Temporal isolation explains host-related genetic differentiation in a group of widespread mycoparasitic fungi. Mol Ecol 20:1492–1507CrossRefPubMedGoogle Scholar
  27. Komatsu T, Akimoto S (1995) Genetic differentiation as a result of adaptation to the phenologies of individual host trees in the galling aphid Kaltenbachiella japonica. Ecol Entomol 20:33–42CrossRefGoogle Scholar
  28. Ladley JJ, Kelly D (1996) Dispersal, germination, and survival of New Zealand mistletoes (Loranthaceae): dependence on birds. NZ J Ecol 20:69–79Google Scholar
  29. Ladley JJ, Kelly D, Robertson AW (1997) Explosive flowering, nectar production, breeding systems, and pollinators of New Zealand mistletoes (Loranthaceae). NZ J Bot 35:345–360CrossRefGoogle Scholar
  30. Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103:11211–11216.  https://doi.org/10.1073/pnas.0604755103 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Larson DL (1991) Ecology of desert mistletoe seed dispersal. In: Ph.D thesis, University of Illinois at Chicago, Chicago, ILGoogle Scholar
  32. Larson DL (1996) Seed dispersal by specialist versus generalist foragers: the plant’s perspective. Oikos 76:113–120CrossRefGoogle Scholar
  33. Le Gac M, Giraud T (2004) What is sympatric speciation in parasites? Trend Parasitol 20:207–208.  https://doi.org/10.1016/j.pt.2004.03.005 CrossRefGoogle Scholar
  34. Li J, Corajod J, Deyoung J (2010) Host preferences of beechdrops (Epifagus): evidence from chloroplast DNA sequence data. Mich Bot 49:79–84Google Scholar
  35. Lichter JM, Berry AM (1991) Establishment of the mistletoe Phoradendron macrophyllum: phenology of early stages and host compatibility studies. Bot Gaz 146:468–475CrossRefGoogle Scholar
  36. Linn C, Feder JL, Nojima S, Dambroski HR, Berlocher SH, Roelofs W (2003) Fruit odor discrimination and sympatric host race formation in Rhagoletis. Proc Natl Acad Sci USA 100:11490–11493.  https://doi.org/10.1073/pnas.1635049100 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Lira-Noriega A, Toro-Nunez O, Oaks JR, Mort ME (2015) The roles of history and ecology in chloroplast phylogeographic patterns of the bird-dispersed plant parasite Phoradendron californicum (Viscaceae) in the Sonoran Desert. Am J Bot 102:149–164CrossRefPubMedGoogle Scholar
  38. Marquardt ES, Pennings SC (2010) Constraints on host use by a parasitic plant. Oecol 164:177–184CrossRefGoogle Scholar
  39. Mattsson M, Hood GR, Feder JL, Ruedas LA (2015) Rapid and repeatable shifts in life-history timing of Rhagoletis pomonella (Diptera: Tephritidae) following colonization of novel host plants in the Pacific Northwestern United States. Ecol Evol.  https://doi.org/10.1002/ece3.1826 PubMedPubMedCentralGoogle Scholar
  40. Nickrent DL (2002) Mistletoe phylogenetics: Current relationships gained from analysis of DNA sequences. In: Proceedings of the Western International Forest Disease Work Conference, August 14–18, 2000. Waikoloa, Hawai’i, pp 48–57Google Scholar
  41. Nickrent DL (2011) Santalales (including mistletoes). Encyclopedia of Life Sciences. doi: https://doi.org/10.1002/9780470015902.a0003714.pub2 Google Scholar
  42. Nickrent DL, Duff RJ, Colwell AE, Wolfe AD, Young ND, Steiner KE, de Pamphilis CW (1998) Molecular phylogenetic and evolutionary studies of parasitic plants. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants II. Kluwer, Boston, pp 211–241CrossRefGoogle Scholar
  43. Norton DA, Carpenter MA (1998) Mistletoes as parasites: host specificity and speciation. Trend Ecol Evol 5347:101–105CrossRefGoogle Scholar
  44. Norton DA, De Lange PJ (1999) Host specificity in parasitic mistletoes (Loranthaceae) in New Zealand. Funct Ecol 13:552–559CrossRefGoogle Scholar
  45. Ollerton J, Stott A, Allnutt E, Shove S, Taylor C, Lamborn E (2007) Pollination niche overlap between a parasitic plant and its host. Oecologia 151:473–485.  https://doi.org/10.1007/s00442-006-0605-y CrossRefPubMedGoogle Scholar
  46. Overton JM (1997) Host specialization and partial reproductive isolation in desert mistletoe (Phoradendron californicum). Southwest Nat 42:201–209Google Scholar
  47. Rathcke B (1983) Competition and facilitation among plants for pollination. In: Real L (ed) Pollination biology. Academic Press, London, pp 305–329CrossRefGoogle Scholar
  48. Restrepo C, Sargent S, Levey D, Watson D (2002) The role of vertebrates in the diversification of New World mistletoes. In: Galetti MGM (ed) Seed dispersal and frugivory: ecology, evolution and conservation, 6th edn. CABI Publishing, Wallingford, UK, pp 83–98Google Scholar
  49. Robertson AW, Kelly D, Ladley JJ, Sparrow AD (1999) Effects of pollinator loss on endemic New Zealand mistletoes (Loranthaceae). Cons Bio 13:499–508CrossRefGoogle Scholar
  50. Roxburgh L, Nicolson SW (2005) Patterns of host use in two African mistletoes: the importance of mistletoe-host compatibility and avian disperser behavior. Funct Ecol 19:865–873CrossRefGoogle Scholar
  51. Schulze ED, Ehleringer JR (1984) The effect of nitrogen supply on growth and water-use efficiency of xylem-tapping mistletoes. Planta 162:268–275CrossRefPubMedGoogle Scholar
  52. Simpson JE, Hurtado PJ, Medlock J, Molaei G, Andreadis TG, Galvani AP, Diuk-Wasser MA (2012) Vector host-feeding preferences drive transmission of multi-host pathogens: West Nile virus as a model system. Proc Biol Sci 279:925–933.  https://doi.org/10.1098/rspb.2011.1282 CrossRefPubMedGoogle Scholar
  53. Sobel JM, Chen GF (2014) Unification of methods for estimating the strength of reproductive isolation. Evol 68:1511–1522CrossRefGoogle Scholar
  54. Thurgood CJ, Rumsey FJ, Harris SA, Hiscock SJ (2008) Host-driven divergence in the parasitic plant Orobanche minor Sm. (Orobanchaceae). Mol Ecol 17:4289–4303CrossRefGoogle Scholar
  55. USA National Phenology Network (2015) Plant phenology data for the United States, 2011-01 to 2015-07. In: USA-NPN, Tucson, Arizona, USAGoogle Scholar
  56. van Dongen S, Backeljau T, Matthysen E, Dhondt AA (1997) Synchronization of hatching date with budburst of individual host trees (Quercus robur) in the winter moth (Operophtera brumata) and its fitness consequences. J Anim Ecol 66:113–121.  https://doi.org/10.2307/5969 CrossRefGoogle Scholar
  57. van Ommeren RJ, Whitham TG (2002) Changes in interactions between juniper and mistletoe mediated by shared avian frugivores: parasitism to potential mutualism. Oecologia 130:281–288.  https://doi.org/10.1007/s004420100792 CrossRefPubMedGoogle Scholar
  58. Walsberg GE (1975) Digestive adaptations of Phainopepla nitens associated with the eating of mistletoe berries. Condor 77:169–174CrossRefGoogle Scholar
  59. Walsberg GE (1977) Ecology and energetics of contrasting social systems in Phainopepla nitens (Aves: Ptilogonatidae). University of California Press, OaklandGoogle Scholar
  60. Wiens JJ, Lapoint RT, Whiteman NK (2015) Herbivory increases diversification across insect clades. Nat Commun 6:8370.  https://doi.org/10.1038/ncomms9370 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Wiesenborn WD (2016) Conspecific pollen loads on insects visiting female flowers on parasitic Phoradendron californicum (Viscaceae). West North Am Nat 76:113–121CrossRefGoogle Scholar
  62. Yule KM, Koop JAH, Alexandre NM, Johnston LR, Whiteman NK (2016) Population structure of a vector-borne plant parasite. Mol Ecol 25:3332–3343CrossRefPubMedGoogle Scholar
  63. Zitzer SF, Archer SR, Boutton TW (1996) Spatial variability in the potential for symbiotic N2 fixation by woody plants in a subtropical savanna ecosystem. J Appl Ecol 33:1125–1136CrossRefGoogle Scholar
  64. Zuber D, Widmer A (2009) Phylogeography and host race differentiation in the European mistletoe (Viscum album L.). Mol Ecol 18:1946–1962CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA

Personalised recommendations