Convergent and divergent evolution in carnivorous pitcher plant traps

New Phytologist

Volumn 217, Issue 3, 2018, Pages 1035-1041

  Thorogood, Chris J ^a   Bauer, Ulrike ^b   Hiscock, Simon J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

adaptive radiation; Cephalotus; functional morphology; Nepenthes; Sarraceniaceae; speciation

Indexed keywords

ADAPTIVE RADIATION; CARNIVOROUS PLANT; CONVERGENT EVOLUTION; DIVERGENCE; FUNCTIONAL MORPHOLOGY; SPECIATION (BIOLOGY); TRAPPING;

CEPHALOTUS; NEPENTHES; SARRACENIACEAE;

ADAPTATION; EVOLUTION; PHYSIOLOGY; SARRACENIACEAE; SPECIES DIFFERENTIATION; ULTRASTRUCTURE;

ADAPTATION, PHYSIOLOGICAL; BIOLOGICAL EVOLUTION; GENETIC SPECIATION; SARRACENIACEAE;

EID: 85040724689     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.14879     Document Type: Review

References (53)

1. Bauer U, Bohn HF, Federle W. 2008. Harmless nectar source or deadly trap: Nepenthes pitchers are activated by rain, condensation and nectar. Proceedings of the Royal Society B 275: 259–265.
2. Bauer U, Clemente CJ, Renner T, Federle W. 2012. Form follows function: morphological diversification and alternative trapping strategies in carnivorous Nepenthes pitcher plants. Journal of Evolutionary Biology 25: 90–102.
3. Bauer U, Federle W, Seidel H, Grafe TU, Ioannou CC. 2015b. How to catch more prey with less effective traps: explaining the evolution of temporarily inactive traps in carnivorous pitcher plants. Proceedings of the Royal Society B: Biological Sciences 282: 20142675.
4. Bauer U, Paulin M, Robert D, Sutton GP. 2015a. Mechanism for rapid passive-dynamic prey capture in a pitcher plant. PNAS 112: 13384–13389.
5. Bauer U, Rembold K, Grafe TU. 2016. Carnivorous Nepenthes pitcher plants are a rich food source for a diverse vertebrate community. Journal of Natural History 50: 483–495.
6. Bauer U, Scharmann M, Skepper J, Federle W. 2013. ‘Insect aquaplaning’ on a superhydrophilic hairy surface: how Heliamphora nutans Benth. pitcher plants capture prey. Proceedings of the Royal Society B: Biological Sciences 280: 20122569.
7. Bazile V, Moran JA, Le Moguédec G, Marshall DJ, Gaume L. 2012. A carnivorous plant fed by its ant symbiont: a unique multi-faceted nutritional mutualism. PLoS ONE 7: e36179.
8. Bemm F, Becker D, Larisch C, Kreuzer I, Escalante-Perez M, Schulze WX, Ankenbrand M, Van de Weyer A-L, Krol E, Al-Rasheid KA et al. 2016. Venus flytrap carnivorous lifestyle builds on herbivore defense strategies. Genome Research 26: 1–14.
9. Bittleston LS, Pierce NE, Ellison AM, Pringle A. 2016. Convergence in multispecies interactions. Trends in Ecology & Evolution 31: 269–280.
10. Bohn HF, Federle W. 2004. Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface. Proceedings of the National Academy of Sciences, USA 101: 14138–14143.
11. Bonhomme V, Gounand I, Alaux C, Jousselin E, Barthelemy D, Gaume L. 2010. The plant-ant Camponotus schmitzi helps its carnivorous host-plant Nepenthes bicalcarata to catch its prey. Journal of Tropical Ecology 27: 15–24.
12. Bonhomme V, Pelloux-Prayer H, Jousselin E, Forterre Y, Labat JJ, Gaume L. 2011. Slippery or sticky? Functional diversity in the trapping strategy of Nepenthes carnivorous plants. New Phytologist 191: 545–554.
13. Chapman MA, Hiscock SJ, Filatov DA. 2016. The genomic bases of morphological divergence and reproductive isolation driven by ecological speciation in Senecio (Asteraceae). Journal of Evolutionary Biology 29: 98–113.
14. Chin L, Chung AY, Clarke CM. 2014. Interspecific variation in prey capture behavior by co-occurring Nepenthes pitcher plants – evidence for resource partitioning or sampling-scheme artefacts? Plant Signaling and Behavior 9: e27930.
15. Chin L, Moran JA, Clarke CM. 2010. Trap geometry in three giant montane pitcher plant species from Borneo is a function of tree shrew body size. New Phytologist 186: 461–470.
16. Clarke CM, Bauer U, Lee CC, Tuen AA, Rembold K, Moran JA. 2009. Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant. Biology Letters 5: 632–635.
17. Clarke CM, Moran JA. 2016. Climate, soils and vicariance – their roles in shaping the diversity and distribution of Nepenthes in Southeast Asia. Plant and Soil 403: 37–51.
18. Darwin C. 1875. Insectivorous plants. London, UK: John Murray.
19. Di Giusto B, Grosbois V, Fargeas E, Marshall DJ, Gaume L. 2008. Contribution of pitcher fragrance and fluid viscosity to high prey diversity in a Nepenthes carnivorous plant from Borneo. Journal of Biosciences 33: 121–136.
20. Ellison AM, Gotelli NJ. 2001. Evolutionary ecology of carnivorous plants. Trends in Ecology and Evolution 16: 623–629.
21. Filatov DA, Osborne OG, Papadopulos AS. 2016. Demographic history of ecological speciation in Senecio altitudinal hybrid zone on Mt. Etna. Molecular Ecology 25: 2467–2481.
22. Fukushima K, Fang X, Alvarez-Ponce D, Cai H, Carretero-Paulet L, Chen C, Chang TH, Farr KM, Fujita T, Hiwatashi Y et al. 2017. Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory. Nature Ecology & Evolution 1: 59.
23. Fukushima K, Fujita H, Yamaguchi T, Kawaguchi M, Tsukaya H, Hasebe M. 2015. Oriented cell division shapes carnivorous pitcher leaves of Sarracenia purpurea. Nature Communications 6: 6450.
24. Gaume L, Forterre Y. 2007. A viscoelastic deadly fluid in carnivorous pitcher plants. PLoS ONE 2: e1185.
25. Gaume L, Perret P, Gorb E, Gorb S, Labat JJ, Rowe N. 2004. How do plant waxes cause flies to slide? Experimental tests of wax-based trapping mechanisms in three pitfall carnivorous plants. Arthropod Structure & Development 33: 103–111.
26. Givnish TJ. 2015. New evidence on the origin of carnivorous plants. Proceedings of the National Academy of Sciences, USA 112: 10–11.
27. Godwin J, Fautin DG. 1992. Defense of host actinians by anemonefishes. Copeia 3: 902–908.
28. Grafe TU, Schöner CR, Kerth G, Junaidi A, Schöner MG. 2011. A novel resource–service mutualism between bats and pitcher plants. Biology Letters 7: 436–439.
29. Heubl G, Bringmann G, Meimberg H. 2006. Molecular phylogeny and character evolution of carnivorous plant families in caryophyllales – revisited. Plant Biology 8: 821–830.
30. Juniper BE, Robins RJ, Joel DM. 1989. The carnivorous plants. London, UK: Academic Press.
31. Lim YS, Schöner CR, Schöner MG, Kerth G, Thornham DG, Scharmann M, Grafe TU. 2015. How a pitcher plant facilitates roosting of mutualistic woolly bats. Evolutionary Ecology Research 16: 581–591.
32. Meimberg H, Dittrich P, Bringmann G, Schlauer J, Heubl G. 2000. Molecular phylogeny of Caryophyllidae s.l. based on MatK sequences with special emphasis on carnivorous taxa. Plant Biology 2: 218–228.
33. Meimberg H, Heubl G. 2006. Introduction of a nuclear marker for phylogenetic analysis of Nepenthaceae. Plant Biology 8: 831–840.
34. Meimberg H, Wistuba A, Dittrich P, Heubl G. 2001. Molecular phylogeny of Nepenthaceae based on cladistic analysis of plastid trnK intron sequence data. Plant Biology 3: 164–175.
35. Merbach MA, Zizka G, Fiala B, Merbach D, Booth WE, Maschwitz U. 2007. Why a carnivorous plant cooperates with an ant – selective defence against pitcher-destroying weevils in the myrmecophytic pitcher plant Nepenthes bicalcarata Hook. F. Ecotropica 13: 45–56.
36. Moran JA, Clarke CM. 2010. The carnivorous syndrome in Nepenthes pitcher plants: current state of knowledge and potential future directions. Plant Signalling and Behaviour 5: 644–648.
37. Moran JA, Clarke CM, Hawkins BJ. 2003. From carnivore to detritivore? Isotopic evidence for leaf litter utilization by the tropical pitcher plant Nepenthes ampullaria. International Journal of Plant Science 164: 635–639.
38. Moran JA, Gray LK, Clarke CM, Chin L. 2013. Capture mechanism in Palaeotropical pitcher plants (Nepenthaceae) is constrained by climate. Annals of Botany 112: 1279–1291.
39. Moran JA, Merbach MA, Livingston NJ, Clarke CM, Booth WE. 2001. Termite prey specialization in the pitcher plant Nepenthes albomarginata. Evidence from stable isotope analysis. Annals of Botany 88: 307–311.
40. Moran JA, Moran AJ. 1998. Foliar reflectance and vector analysis reveal nutrient stress in prey-deprived pitcher plants (Nepenthes rafflesiana). International Journal of Plant Sciences 159: 996–1001.
41. Pavlovic A. 2012. Adaptive radiation with regard to nutrient sequestering strategies in the carnivorous plants of the genus Nepenthes. Plant Signalling and Behaviour 7: 295–297.
42. Peng HS, Clarke CM. 2015. Prey capture patterns in Nepenthes species and natural hybrids – are the pitchers of hybrids as effective at trapping prey as those of their parents? Carnivorous Plant Newsletter 44: 62–79.
43. Renner T, Specht CD. 2013. Inside the trap: gland morphologies, digestive enzymes, and the evolution of plant carnivory in the Caryophyllales. Current Opinion in Plant Biology 16: 436–442.
44. Schaefer HM, Ruxton GD. 2014. Fenestration: a window of opportunity for carnivorous plants. Biology Letters 10: 20140134.
45. Scharmann M, Thornham DG, Grafe TU, Federle W. 2013. A novel type of nutritional ant–plant interaction: ant partners of carnivorous pitcher plants prevent nutrient export by dipteran pitcher infauna. PLoS ONE 8: e63556.
46. Schluter D. 2000. The ecology of adaptive radiation. Oxford, UK: Oxford University Press.
47. Scholz I, Bückins M, Dolge L, Erlinghagen T, Weth A, Hischen F, Mayer J, Hoffmann S, Riederer M, Riedel M et al. 2010. Slippery surfaces of pitcher plants: Nepenthes wax crystals minimize insect attachment via microscopic surface roughness. Journal of Experimental Biology 213: 1115–1125.
48. Schöner MG, Schöner CR, Simon R, Grafe TU, Puechmaille SJ, Ji LL, Kerth G. 2015. Bats are acoustically attracted to mutualistic carnivorous plants. Current Biology 25: 1911–1916.
49. Schulte K, Barfuss MHJ, Zizka G. 2009. Phylogeny of Bromelioideae (Bromeliaceae) inferred from nuclear and plastid DNA loci reveals the evolution of the tank habit within the subfamily. Molecular Phylogenetics & Evolution 51: 327–339.
50. Stephens JD, Rogers WL, Heyduk K, Cruse-Sanders JM, Determann RO, Glenn TC, Malmberg RL. 2015. Resolving phylogenetic relationships of the recently radiated carnivorous plant genus Sarracenia using target enrichment. Molecular Phylogenetics and Evolution 85: 76–87.
51. Thornham DG, Smith JM, Grafe TU, Federle W. 2012. Setting the trap: cleaning behaviour of Camponotus schmitzi ants increases long-term capture efficiency of their pitcher plant host, Nepenthes bicalcarata. Functional Ecology 26: 11–19.
52. Thorogood CJ. 2010. The Malaysian Nepenthes: evolutionary and taxonomic perspectives. New York, NY, USA: Nova Publishers.
53. Whittall JB, Hodges SA. 2007. Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature Letters 447: 706–710.