Cost of resistance to trematodes in freshwater snail populations with low clonal diversity
Tóm tắt
The persistence of high genetic variability in natural populations garners considerable interest among ecologists and evolutionary biologists. One proposed hypothesis for the maintenance of high levels of genetic diversity relies on frequency-dependent selection imposed by parasites on host populations (Red Queen hypothesis). A complementary hypothesis suggests that a trade-off between fitness costs associated with tolerance to stress factors and fitness costs associated with resistance to parasites is responsible for the maintenance of host genetic diversity. The present study investigated whether host resistance to parasites is traded off with tolerance to environmental stress factors (high/low temperatures, high salinity), by comparing populations of the freshwater snail Melanoides tuberculata with low vs. high clonal diversity. Since polyclonal populations were found to be more parasitized than populations with low clonal diversity, we expected them to be tolerant to environmental stress factors. We found that clonal diversity explained most of the variation in snail survival under high temperature, thereby suggesting that tolerance to high temperatures of clonally diverse populations is higher than that of populations with low clonal diversity. Our results suggest that resistance to parasites may come at a cost of reduced tolerance to certain environmental stress factors.
Tài liệu tham khảo
Grenfell BT, Dobson AP. Ecology of infectious diseases in natural populations. Cambridge: Cambridge University Press; 1995.
Gillespie JH. Natural selection for resistance to epidemics. Ecology. 1975;56:493–5.
May RM, Anderson RM. Epidemiology and genetics in the coevolution of parasites and hosts. Proc R Soc B. 1983;219:281–313.
Antonovics J, Thrall PH. The cost of resistance and the maintenance of genetic polymorphism in host-pathogen systems. Proc R Soc B. 1994;257:105–10.
Frank SA. Coevolutionary genetics of hosts and parasites with quantitative inheritance. Evol Ecol. 1994;8:74–94.
Boots M, White A, Best A, Bowers R. The importance of who infects whom: the evolution of diversity in host resistance to infectious disease. Ecol Lett. 2012;15:1104–11.
Råberg L, Sim D, Read AF. Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science. 2007;318:812–4.
Fritz RS, Simms EL. Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. Chicago: University of Chicago Press; 1992.
Webster JP, Woolhouse MEJ. Cost of resistance: relationship between reduced fertility and increased resistance in a snail—schistosome host—parasite system. Proc R Soc B. 1999;266:391–6.
Lohse K, Gutierrez A, Kaltz O. Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata. Evolution. 2006;60:1177–86.
Dallas T, Holtackers M, Drake JM. Costs of resistance and infection by a generalist pathogen. Ecol Evol. 2016;6:1737–44.
Hasu T, Benesh DP, Valtonen ET. Differences in parasite susceptibility and costs of resistance between naturally exposed and unexposed host populations. J Evol Biol. 2009;22:699–707.
Auld SKJR, Penczykowski RM, Housley Ochst J, Grippt DC, Hall SR, Duffy MA. Variation in costs of parasite resistance among natural host populations. J Evol Biol. 2013;26:2479–86.
Guttel Y, Ben-Ami F. The maintenance of hybrids by parasitism in a freshwater snail. Int J Parasitol. 2014;44:1001–8.
Dagan Y, Liljeroos K, Jokela J, Ben-Ami F. Clonal diversity driven by parasitism in a freshwater snail. J Evol Biol. 2013;26:2509–19.
Lively CM, Howard RS. Selection by parasites for clonal diversity and mixed mating. Philos Trans R Soc Lond B. 1994;346:271–81.
King KC, Jokela J, Lively CM. Parasites, sex and clonal diversity in natural snail populations. Evolution. 2011;65:1474–81.
Pointier JP. Invading freshwater gastropods: some conflicting aspects for public health. Malacologia. 1999;41:403–11.
Facon B, Pointier JP, Glaubrecht M, Poux C, Jarne P, David P. A molecular phylogeography approach to biological invasions of the New World by parthenogenetic Thiarid snails. Mol Ecol. 2003;12:3027–39.
Ben-Ami F. First report of the invasive freshwater snail Tarebia granifera (Lamarck, 1816) (Gastropoda: Thiaridae) from Israel. Nautilus. 2006;120:156–61.
Livshits G, Fishelson L. Biology and reproduction of the freshwater snail Melanoides tuberculata (Gastropoda: Prosobranchia) in Israel. Isr J Zool. 1983;32:21–35.
Dudgeon D. The life cycle, population dynamics and productivity of Melanoides tuberculata (Muller, 1774) (Gastropoda: Prosobranchia: Thiaridae) in Hong Kong. J Zool. 1986;208:37–53.
Jacob J. Cytological studies of Melaniidae (Mollusca) with special reference to parthenogenesis and polyploidy. I. Oogenesis of the parthenogenetic species of Melanoides (Prosobranchia-Gastropoda). Trans R Soc Edinb. 1957;63:341–52.
Jacob J. Cytological studies of Melaniidae (Mollusca) with special reference to parthenogenesis and polyploidy. II. A study of meiosis in the rare males of the polyploid race of Melanoides tuberculatus and Melanoides lineatus. Trans R Soc Edinb. 1958;63:433–44.
Berry AJ, Kadri AH. Reproduction in the Malayan freshwater cerithiacean gastropod Melanoides tuberculata. J Zool. 1974;172:369–81.
Samadi S, Mavárez J, Pointier JP, Delay B, Jarne P. Microsatellite and morphological analysis of population structure in the parthenogenetic freshwater snail Melanoides tuberculata: insights into the creation of clonal variability. Mol Ecol. 1999;8:1141–53.
Heller J, Farstay V. Sexual and parthenogenetic populations of the freshwater snail Melanoides tuberculata in Israel. Isr J Zool. 1990;37:75–87.
Ben-Ami F, Heller J. Spatial and temporal patterns of parthenogenesis and parasitism in the freshwater snail Melanoides tuberculata. J Evol Biol. 2005;18:138–46.
Ben-Ami F, Heller J. Temporal patterns of geographic parthenogenesis in a freshwater snail. Biol J Linn Soc. 2007;91:711–8.
Ben-ami F, Heller J. Sex versus parasitism versus density. Biol J Linn Soc. 2008;93:537–44.
Facon B, Jarne P, Pointier JP, David P. Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance. J Evol Biol. 2005;18:524–35.
Facon B, Pointier JP, Jarne P, Sarda V, David P. High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Curr Biol. 2008;18:363–7.
Radev V, Kanev I, Gold D. Life cycle and identification of an eyefluke from Israel transmitted by Melanoides tuberculata (Müller, 1774). J Parasitol. 2000;86:773–6.
Dzikowski R, Diamant A, Paperna I. Trematode metacercariae of fishes as sentinels for a changing limnological environment. Dis Aquat Organ. 2003;55:145–50.
Ben-Ami F, Gold D, Fried B. Differential infectivity of Transversotrema patialense for naive fish. J Parasitol. 2005;91:949–50.
Yousif F, Ibrahim A, El-Bardicy S, Sleem S, Ayoub M. Morphology of new eleven cercariae procured from Melanoides Tuberculata snails in Egypt. Aust J Basic Appl Sci. 2010;4:1482–94.
Pinto HA, De Melo AL. A checklist of trematodes (Platyhelminthes) transmitted by Melanoides tuberculata (Mollusca: Thiaridae). Zootaxa. 2011;28:15–28.
Farstay V. Centrocestus sp. (Heterophyidae) and other trematode infections of the snail Melanoides tuberculata (Müller, 1774) and cichlid fish in Lake Kinneret. M.Sc. thesis. Jerusalem: The Hebrew University; 1986.
Heller J, Farstay V. A field method to separate males and females of the freshwater snail Melanoides tuberculata. J Molluscan Stud. 1989;55:427–9.
Shannon C. A mathematical theory of communication. Bell Syst Tech J. 1948;27:379–423.
Kosman E, Leonard K. Conceptual analysis of methods applied to assessment of diversity within and distance between populations with asexual or mixed mode of reproduction. New Phytol. 2007;174:683–96.
Kosman E. Measuring diversity: from individuals to populations. Eur J Plant Pathol. 2014;138:467–86.
Schachtel G, Dinoor A, Herrmann A, Kosman E. Comprehensive evaluation of virulence and resistance data: a new analysis tool. Plant Dis. 2012;96:1060–3.
Yang JS, Nam HJ, Seo M, Han SK, Choi Y, Nam HG, et al. OASIS: online application for the survival analysis of lifespan assays performed in aging research. PLoS ONE. 2011;6:e23525.
Seppälä O, Langeloh L. Estimating genetic and maternal effects determining variation in immune function of a mixed-mating snail. PLoS ONE. 2016;11:e0161584.
Parsell DA, Lindquist S. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet. 1993;27:437–96.
Parsell DA, Lindquist S. Heat shock proteins and stress tolerance. In: Morimoto R, Tissieres A, Georgopoulos C, editors. The biology of heat shock proteins and molecular chaperones. New York: Cold Spring Harbor Laboratory Press; 1994. p. 457–94.
Tomanek L, Somero GN. Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography. J Exp Biol. 1999;202:2925–36.
Roessler MA, Beardsley GL, Tabb DC. New records of the introduced snail, Melanoides tuberculata (Mollusca: Thiaridae) in south Florida. Fla Sci. 1977;40:87–94.
Englund RA. The loss of native biodiversity and continuing nonindigenous species introductions in freshwater, estuarine, and wetland communities of Pearl Harbor, Oahu, Hawaiian Islands. Estuaries. 2002;25:418–30.
Wingard GL, Murray JB, Schill WB, Phillips EC. Red-rimmed Melania (Melanoides tuberculatus)-a snail in Biscayne National Park, Florida-harmful invader or just a nuisance? In: fact sheet 2008-3006. US Geological Survey. 2008. https://pubs.usgs.gov/fs/2008/3006. Accessed 15 Mar 2017.
Vogler RE, Núñez V, Gregoric DG, Beltramino AA, Peso JG. Melanoides tuberculata: the history of an invader. In: Hämäläinen EM, Järvinen S, editors. Snails biology, ecology and conservation. New York: Nova Science Publishers; 2012. p. 65–85.
Farani GL, Nogueira MM, Johnsson R, Neves E. The salt tolerance of the freshwater snail Melanoides tuberculata (Mollusca, Gastropoda), a bioinvader gastropod. Panam J Aquat Sci. 2015;10:212–21.
Jacobsen R, Forbes VE. Clonal variation in life-history traits and feeding rates in the gastropod, Potamopyrgus antipodarum: performance across a salinity gradient. Funct Ecol. 1997;11:260–7.