Annals of Occupational and Environmental Medicine | |
Detection experiments with humans implicate visual predation as a driver of colour polymorphism dynamics in pygmy grasshoppers | |
Einat Karpestam2  Sami Merilaita1  Anders Forsman2  | |
[1] Behavioural and Evolutionary Ecology Group, Environmental and Marine Biology, Department of Biosciences, Åbo Akademi University, Turku, FI-20520, Finland | |
[2] Ecology and Evolution in Microbial Model Systems, EEMIS, Department of Biology and Environmental Science, Linnaeus University, Kalmar, SE-391 82, Sweden | |
关键词: Tetrix subulata; Evolution; Predation; Crypsis; Colour polymorphism; Camouflage; Biodiversity; | |
Others : 1085409 DOI : 10.1186/1472-6785-13-17 |
|
received in 2012-11-15, accepted in 2013-04-16, 发布年份 2013 | |
【 摘 要 】
Background
Animal colour patterns offer good model systems for studies of biodiversity and evolution of local adaptations. An increasingly popular approach to study the role of selection for camouflage for evolutionary trajectories of animal colour patterns is to present images of prey on paper or computer screens to human ‘predators’. Yet, few attempts have been made to confirm that rates of detection by humans can predict patterns of selection and evolutionary modifications of prey colour patterns in nature. In this study, we first analyzed encounters between human ‘predators’ and images of natural black, grey and striped colour morphs of the polymorphic Tetrix subulata pygmy grasshoppers presented on background images of unburnt, intermediate or completely burnt natural habitats. Next, we compared detection rates with estimates of capture probabilities and survival of free-ranging grasshoppers, and with estimates of relative morph frequencies in natural populations.
Results
The proportion of grasshoppers that were detected and time to detection depended on both the colour pattern of the prey and on the type of visual background. Grasshoppers were detected more often and faster on unburnt backgrounds than on 50% and 100% burnt backgrounds. Striped prey were detected less often than grey or black prey on unburnt backgrounds; grey prey were detected more often than black or striped prey on 50% burnt backgrounds; and black prey were detected less often than grey prey on 100% burnt backgrounds. Rates of detection mirrored previously reported rates of capture by humans of free-ranging grasshoppers, as well as morph specific survival in the wild. Rates of detection were also correlated with frequencies of striped, black and grey morphs in samples of T. subulata from natural populations that occupied the three habitat types used for the detection experiment.
Conclusions
Our findings demonstrate that crypsis is background-dependent, and implicate visual predation as an important driver of evolutionary modifications of colour polymorphism in pygmy grasshoppers. Our study provides the clearest evidence to date that using humans as ‘predators’ in detection experiments may provide reliable information on the protective values of prey colour patterns and of natural selection and microevolution of camouflage in the wild.
【 授权许可】
2013 Karpestam et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150113173058618.pdf | 890KB | download | |
Figure 5. | 36KB | Image | download |
Figure 4. | 54KB | Image | download |
Figure 3. | 34KB | Image | download |
Figure 2. | 157KB | Image | download |
Figure 1. | 32KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
【 参考文献 】
- [1]Mappes J, Marples N, Endler JA: The complex business of survival by aposematism. Trends Ecol Evol 2005, 20(11):598-603.
- [2]Ruxton GD, Sherratt TN, Speed M: Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. Oxford: Oxford University Press; 2004.
- [3]Stevens M, Merilaita S: Animal camouflage: current issues and new perspectives. Phil Trans R Soc B 2009, 364:423-427.
- [4]Hoekstra HE, Drumm KE, Nachman MW: Ecological genetics of adaptive color polymorphism in pocket mice: geographic variation in selected and neutral genes. Evolution 2004, 58(6):1329-1341.
- [5]Forsman A: Opposing fitness consequences of color pattern in male and female snakes. J Evol Biol 1995, 8(1):53-70.
- [6]Pellissier L, Wassef J, Bilat J, Brazzola G, Buri P, Colliard C, Fournier B, Hausser J, Yannic G, Perrin N: Adaptive colour polymorphism of Acrida ungarica H. (Orthoptera: Acrididae) in a spatially heterogeneous environment. Acta Oecol 2011, 37(2):93-98.
- [7]Forsman A, Karlsson M, Wennersten L, Johansson J, Karpestam E: Rapid evolution of fire melanism in replicated populations of pygmy grasshoppers. Evolution 2011, 65(9):2530-2540.
- [8]Kettlewell HBD: A resume of investigations on the evolution of melanism in the lepidoptera. Proc R Soc B 1956, 145(920):297-303.
- [9]Cook LM, Cowie RH, Jones JS: Change in morph frequency in the snail Cepaea nemoralis on the Marlborough Downs. Heredity 1999, 82:336-342.
- [10]Ozgo M: Rapid evolution in unstable habitats: a success story of the polymorphic land snail Cepaea nemoralis (Gastropoda: Pulmonata). Biol J Linn Soc 2011, 102(2):251-262.
- [11]Roberts JL, Brown JL, Schulte R, Arizabal W, Summers K: Rapid diversification of colouration among populations of a poison frog isolated on sky peninsulas in the central cordilleras of Peru. J Biogeogr 2007, 34(3):417-426.
- [12]Hughes JM, Mather PB: Evidence for predation as a factor in determining shell color frequencies in a mangrove snail littorina sp (prosobranchia, littorinidae). Evolution 1986, 40(1):68-77.
- [13]Bonte D, Maelfait JP: Colour variation and crypsis in relation to habitat selection in the males of the crab spider Xysticus sabulosus (Hahn, 1832) (Araneae : Thomisidae). Belg J Zool 2004, 134(2):3-7.
- [14]Merilaita S: Habitat heterogeneity, predation and gene flow: colour polymorphism in the isopod. Idotea baltica. Evol Ecol 2001, 15(2):103-116.
- [15]Nosil P, Sandoval CP, Crespi BJ: The evolution of host preference in allopatric vs. parapatric populations of Timema cristinae walking-sticks. J Evol Biol 2006, 19(3):929-942.
- [16]Sandoval CP: Differential visual predation on morphs of Timema cristinae (phasmatodeae, timemidae) and its consequences for host-range. Biol J Linn Soc 1994, 52(4):341-356.
- [17]Tsurui K, Honma A, Nishida T: Camouflage effects of various colour-marking morphs against different microhabitat backgrounds in a polymorphic pygmy grasshopper tetrix japonica. PLoS One 2010, 5(7):e11446.
- [18]Bond AB, Kamil AC: Visual predators select for crypticity and polymorphism in virtual prey. Nature 2002, 415(6872):609-613.
- [19]Byers BA: Habitat-choice polymorphism associated with cryptic shell-color polymorphism in the limpet lottia-digitalis. Veliger 1989, 32(4):394-402.
- [20]Endler JA: Natural-selection on color patterns in poecilia-reticulata. Evolution 1980, 34(1):76-91.
- [21]Endler JA: Natural selection in the wild. Princeton, NJ: Princeton University Press; 1986.
- [22]Kawecki TJ, Ebert D: Conceptual issues in local adaptation. Ecol Lett 2004, 7:1225-1241.
- [23]Arnold SJ, Wade MJ: On the measurement of natural and sexual selection: theory. Evolution 1984, 38(4):709-719.
- [24]Gendron RP, Staddon JER: A laboratory simulation of foraging behavior: the effect of search rate on the probability of detecting prey. Am Nat 1984, 124(3):407-415.
- [25]Penney HD, Hassall C, Skevington JH, Abbott KR, Sherratt TN: A comparative analysis of the evolution of imperfect mimicry. Nature 2012, 483(7390):461-464.
- [26]Beatty CD, Bain RS, Sherratt TN: The evolution of aggregation in profitable and unprofitable prey. Anim Behav 2005, 70:199-208.
- [27]Todd PA: Testing for camouflage using virtual prey and human ‘predators’. J Biol Edu 2009, 43:81-84.
- [28]Karpestam E, Merilaita S, Forsman A: Reduced predation risk for melanistic pygmy grasshoppers in post-fire environments. Ecol & Evol 2012, 2:2204-2212.
- [29]Forsman A, Appelqvist S: Experimental manipulation reveals differential effects of colour pattern on survival in male and female pygmy grasshoppers. J Evol Biol 1999, 12(2):391-401.
- [30]Holst KT: The Saltatoria of Northern Europe. Fauna Entomol Scand 1986, 16:1-127.
- [31]Rehn JAG, Grant HJJ: Tetrix subulata (Orthoptera; Acridoidea; Tetrigidae) as occurring in North America. Proc Acad Nat Sci Phila 1955, 107:145-165.
- [32]Forsman A, Appelqvist S: Visual predators impose correlational selection on prey color pattern and behavior. Behav Ecol 1998, 9(4):409-413.
- [33]Civantos E, Ahnesjö J, Forsman A, Martin J, Lopez P: Indirect effects of prey coloration on predation risk: pygmy grasshoppers versus lizards. Evol Ecol Res 2004, 6(2):201-213.
- [34]Merilaita S, Tuomi J, Jormalainen V: Optimization of cryptic coloration in heterogeneous habitats. Biol J Linn Soc 1999, 67:151-161.
- [35]Levene H: Genetic equilibrium when more than one niche is available. Am Nat 1953, 87:331-333.
- [36]Levins R: Evolution in changing environments. Princeton: Princeton University Press; 1968.
- [37]Hedrick PW: Genetic polymorphism in heterogeneous environments: The age of genomics. Ann Rev Ecol Syst 2006, 37:67-93.
- [38]Frank SA, Slatkin M: Evolution in a variable environment. Am Nat 1990, 136(2):244-260.
- [39]Merilaita S: Crypsis through disruptiv coloration in an isopod. Proc R Soc B 1998, 265:1059-1064.
- [40]Cuthill IC, Stevens M, Sheppard J, Maddocks T, Párraga CA, Troscianko TS: Disruptive coloration and background pattern matching. Nature 2005, 434:72-74.
- [41]Skelhorn J, Rowland HM, Ruxton GD: The evolution and ecology of masquerade. Biol J Linn Soc 2010, 99(1):1-8.
- [42]Kjernsmo K, Merilaita S: Background choice as an anti-predator strategy: the roles of background matching and visual complexity in the habitat choice of the least killifish. Proc R Soc B 2012, 279:4192-4198.
- [43]Gillis JE: Substrate color-matching cues in the cryptic grasshopper Circotettix rabula rabula (Rehn and Hebard). Anim Behav 1982, 30:113-116.
- [44]Ahnesjö J, Forsman A: Differential habitat selection by pygmy grasshopper color morphs; interactive effects of temperature and predator avoidance. Evol Ecol 2006, 20(3):235-257.
- [45]Karpestam E, Forsman A: Dietary differences among colour morphs of pygmy grasshoppers revealed by behavioural experiments and stable isotopes. Evol Ecol Res 2011, 13:461-477.
- [46]Caesar S, Karlsson M, Forsman A: Diversity and relatedness enhance survival in colour polymorphic grasshoppers. PLoS One 2010, 5(5):e10880.
- [47]Bock CE, Bock JH, Grant MC: Effects of bird predation on grasshopper densities in an arizona grassland. Ecology 1992, 73(5):1706-1717.
- [48]King RB: Colour pattern polymorphism in the Lake Erie water snake, Nerodia sipedon insularum. Evolution 1987, 41:241-255.