Research

The persistence of sexual reproduction in natural populations remains as one of the major unsolved problems for evolutionary biology. The problem stems from the fact that male-producing, sexual populations are subject to invasion and rapid replacement by clonal females. In fact, a population of one million sexual individuals would be replaced in less than 50 generations by a clone beginning with a single asexual female. Why, then, is there sex?

A similar paradox exists for recombination. The effect of recombination is to break up the non-random associations between alleles at different loci. Why would this be favored by selection, especially if these associations (linkage disequilibria) were generated by selection in the previous generations? Why break up a good thing?

Over 20 hypotheses have been suggested to explain the evolutionary stability of sexual reproduction, most of which focus on the possible advantages gained by the production of variable offspring. Many of these ideas also apply to recombination. The solution seems far from certain, but most of the effort at present is focused on two general areas: the advantages of sex in clearing deleterious mutations, and the advantages of sex in variable environments. We have been engaged in both empirical and theoretical studies of these hypotheses.

Empirical studies. We work on a New Zealand snail in order to contrast the predictions of the leading theories. The snail is useful for this purpose because sexual and asexual females exist, and often coexist in the same (mixed) population (more about the snail). We have taken a strong-inference approach of forcing the different theories to make different falsifiable predictions, which can be evaluated using biogeographic and/or experimental evidence. Our work to date has been inconsistent with many of the leading hypotheses, but we have been unable to falsify the idea that coevolution with parasites provides an advantage to cross-fertilization in hosts, and vice versa (the Red Queen hypothesis). The basic idea behind the Red Queen hypothesis is that parasites will be under strong selection to infect the most common host genotypes. This kind of frequency-dependent selection will favor rare host genotypes, which should increase in frequency over time, eventually becoming common. The parasite is then under selection to infect these previously rare, but now common host genotypes. This sort of coevolutionary interaction easily leads to oscillations in genotypic frequencies in both the host and the parasite. Under the Red Queen hypothesis, sexual reproduction is selected over asexual reproduction as a mechanism to produce variable progeny, some of which may have relatively rare genotypes that are more likely to escape infection.

Relevant publications 

Lively, C.M. 1987. Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature 328:519-521

Lively, C.M., C. Craddock and R.C. Vrijenhoek. 1990. Red Queen hypothesis supported by parasitism in sexual and clonal fish. Nature 344:864-866

Lively, C.M. and D.G. Lloyd. 1990. The cost of biparental sex under individual selection. American Naturalist 135:489-500

Lively, C.M. 1992. Parthenogenesis in a freshwater snail: reproductive assurance versus parasitic release. Evolution 46:907-913.

Howard, R.S. and C.M. Lively. 1994. Parasitism, mutation accumulation and the maintenance of sex. Nature 367:554-557.  (This pdf provides clearer figs. than printed in Nature)

Lively, C.M. and R.S. Howard. 1994. Selection by parasites for clonal diversity and mixed mating. Philosophical Transactions of the Royal Society 346:271-281.

Dybdahl, M.F. and C.M. Lively. 1995. Host-parasite interactions: infection of common clones in natural populations of a freshwater snail (Potamopyrgus antipodarum). Proceedings of the Royal Society, London B 260:99-103.

Jokela, J. and C.M. Lively. 1995. Parasites, sex, and early reproduction in a mixed population of freshwater snails. Evolution 49:1268-1271.

Dybdahl, M.F. and C.M. Lively. 1998. Host-parasite coevolution: evidence for rare advantage and time-lagged selection in a natural population. Evolution 52: 1057-1066.

Howard, R.S. and C.M. Lively. 1998. The maintenance of sex by parasitism and mutation accumulation under epistatic fitness functions. Evolution 52:604-610.

Lively, C.M., E.J. Lyons, A.D. Peters, and J. Jokela. 1998. Environmental stress and the maintenance of sex in a freshwater snail. Evolution 52:1482-1486.

Peters, A.D. and C.M. Lively. 1999. The Red Queen and fluctuating epistasis: a population genetic analysis of antagonistic coevolution. American Naturalist 154:393-405.

Lively, C. M. and J. Jokela. 2002. Temporal and spatial distributions of parasites and sex in a freshwater snail. Evolutionary Ecology Research 4:219-226.

Howard, R. S. and C.M. Lively. 2002. The ratchet and the Red Queen: the maintenance of sex in parasites. Journal of Evolutionary Biology 15:648-656.

Jokela, J., M.F. Dybdahl, and C.M. Lively. 2009. The maintenance of sex, clonal dynamics, and host-parasite coevolution in a mixed population of sexual and asexual snails. American Naturalist 174: S43-S53.

Lively, C. M. 2010. Parasite virulence, host life history, and the costs and benefits of sex. Ecology 91: 3-6.

Lively, C. M. 2010. A review of Red Queen models for the persistence of obligate sexual reproduction. Journal of Heredity 101: S13-S20.

King, K. C., Jokela, J., and Lively, C. M. 2011. Parasites, sex, and clonal diversity in natural snail populations. Evolution 65: 1474-1481.

Lively, C. M. 2011.  The cost of males in non-equilibrium populations. Evolutionary Ecology Research 13: 105-111.

King, K. C., Delph, L. F., Jokela, J., and Lively, C. M. 2011. Coevolutionary hotspots and coldspots for host sex and parasite local adaptation in a snail-trematode interaction. Oikos 120: 1335-1340.

Morran, L. T., Schmidt, O. G., Gelarden, I. A., Parrish R. C. II, and Lively, C. M. 2011. Running with the Red Queen: host-parasite coevolution selects for biparental sex. Science 333: 216-218.

Koskella, B., Vergara, D., and Lively, C. M. 2011. Experimental evolution of sexual host populations in response to parasites. Evolutionary Ecology Research 13:315-322.

Morran, L. T., Gelarden, I. A., Parrish R. C. II, and Lively, C. M. 2013. Temporal dynamics of outcrossing and host mortality rates in host-pathogen experimental coevolution. Evolution 67: 1860-1868.

Vergara, D., Lively, C. M., King, K. C., and Jokela, J. 2013. The geographic mosaic of sex and infection in lake populations of a New Zealand snail at multiple spatial scales. American Naturalist 182: 484-493.

Paczesniak, D., Adolfsson, S., Liljeroos, K., Klappert, K., Lively, C. M., and Jokela, J. 2014. Faster clonal turnover in high-infection habitats provides evidence for parasite-mediated selection. Journal of Evolutionary Biology 27: 417-428.

Vergara, D., Jokela, J., and Lively, C. M. 2014. Infection dynamics in coexisting sexual and asexual populations: support for the Red Queen hypothesis. American Naturalist 184: S22-S30.

Dapper, A. L. and Lively, C. M. 2014. Interlocus sexually antagonistic coevolution can create indirect selection for increased recombination. Evolution 68: 1216–1224.

Morran, L. T., Parrish R. C. II, Gelarden, I. A., Allen, M. B., and Lively, C. M. 2014. Experimental coevolution: rapid local adaptation by parasites depends on host mating system. American Naturalist 184: S91-S100.

Soper, D. M., King, K. C., Vergara, D., and Lively, C.M. 2014. Parasite exposure increases promiscuity in a freshwater snail. Biology Letters 10, 20131091.

Lively, C. M. and Morran, L.T. 2014. The ecology of sexual reproduction. Journal of Evolutionary Biology 27: 1292-1303.

McKone, M. J., A. K. Gibson, D. Cook, L. A. Freymiller, D. Mishkind, A. Quinlan, J. M. York, C. M. Lively, and M. Neiman. 2016. Fine-scale association between parasites and sex in Potamopyrgus antipodarum within a New Zealand lake. New Zealand Journal of Ecology 40: 330-333.

Gibson, A.K., Jokela, J., and Lively, C.M. 2016. Fine-scale covariation between infection prevalence and susceptibility in a natural population. American Naturalist 188: 1-14.

Gibson, A.K., Xu, J., and Lively, C.M. 2016. Fine-scale covariation between sexual reproduction and susceptibility to local parasites in a natural population. Evolution 70: 2049-2060.

Slowinski, S. P., L. T. Morran, R. C. Parrish II, E. R. Cui, A. Bhattacharya, C. M. Lively, P. C. Phillips. 2016. Coevolutionary interactions with parasites constrain the spread of self-fertilization into outcrossing host populations. Evolution 70: 2632-2639.

Gibson, A. K., L. F. Delph, and C. M. Lively. 2017. The two-fold cost of sex: experimental evidence from a natural system. Evolution Letters 1: 6-15.

Neiman, M., Lively, C.M., and Meirmans, S. 2017. Why sex? A pluralist approach revisited. Trends in Ecology and Evolution 32: 589-600.

Gibson, A. K., K. S. Stoy, and C. M. Lively. 2018. Bloody-minded parasites and sex: the effects of fluctuating virulence. Journal of Evolutionary Biology 31: 611-620.

Gibson, A. K., L. F. Delph, D. Vergara, and C. M. Lively. 2018. Periodic, parasite-mediated selection for and against sex. American Naturalist 192: 537-551.

Paczesniak, D., K. Klappert, K. Kopp, M. Neiman, K. Seppälä, C.M. Lively, and J. Jokela. 2019. Parasite resistance predicts fitness better than fecundity in a natural population of the freshwater snail Potamopyrgus antipodarum. Evolution 73: 1634–1646.

Why do some infections make hosts very sick, while other infections are rather benign?  What is the effect of intra-specific competition on the effects of infection?  What is the effect of multiple strain infections on host condition?  These are questions that we are investigating using mathematical models and different biological systems.

Relevant publications

Lively, C.M., S.G. Johnson, L.F. Delph, and K. Clay. 1995. Thinning reduces the effect of rust infection on jewelweed (Impatiens capensis). Ecology 76:1859-1862.

Lively, C.M. 2001. Propagule interactions and the evolution of virulence. Journal of Evolutionary Biology 14:317-324.

Lively, C.M. 2005. Evolution of virulence: coinfection and propagule production in spore–producing parasites. BMC Evolutionary Biology 2005, 5:64.

Lively, C.M. 2006. The ecology of virulence. Ecology Letters 9: 1089-1095.

Bashey, F., L.T. Morran, and C.M. Lively. 2007. Coinfection, kin selection, and the rate of host exploitation by a parasitic nematode. Evolutionary Ecology Research 9: 947-958.

Vigneux, F., F. Bashey, M. Sicard, and C.M. Lively. 2008. Low migration decreases interference competition among parasites and increases virulence. Journal of Evolutionary Biology 21: 1245-1251.

Wolinska, J., K.C. King, F. Vigneux, and C.M. Lively. 2008. Virulence, cultivating conditions, and phylogenetic analyses of oomycete parasites in Daphnia. Parasitology 135: 1667-1678.

Bashey, F. and C.M. Lively. 2009. Group selection on population size affects life-history patterns in the entomopathogenic nematode Steinernema carpocapsae. Evolution 63: 1301-1311.

Lively, C.M. 2009. Local host competition in the evolution of virulence. Journal of Evolutionary Biology 22: 1286-1274.

Lively, C. M. 2009. The maintenance of sex: host-parasite coevolution with density-dependent virulence. Journal of Evolutionary Biology. 22: 2086–2093.

Lively, C. M. 2010. Parasite virulence, host life history, and the costs and benefits of sex. Ecology 91: 3-6.

Hawlena, H., Bashey, F., Mendes-Soares, H, and Lively, C.M. 2010. Spiteful interactions in a natural population of the bacterium Xenorhabdus bovienii. American Naturalist 175: 374-381.

Hawlena, H., Bashey, F., and Lively, C. M. 2010. The evolution of spite: population structure and bacteriocin-mediated antagonism in two natural populations of Xenorhabdus bacteria. Evolution 64: 3198-3204.

Hawlena, H. Bashey, F., and Lively, C. M. 2012. Bacteriocin-mediated interactions within and between coexisting species. Ecology and Evolution 2: 2516-2521.

Bashey, F., Hawlena, H., and Lively, C. M. 2013. Alternative paths to success in a parasite community: within-host competition can favor higher virulence or direct interference. Evolution 67: 900-907.

Do hosts and parasites rapidly evolve in response to each other?  If so, how rapidly: tens of generations, hundreds of generations?  Do parasite become adapted to infect hosts from their local host populations?  These are questions that we have mainly addressed using a freshwater New Zealand snail and its trematode parasites.  But we have also conducted experimental evolution studies on nematodes (lead by Levi Morran).  

Relevant publications

Lively, C.M. 1989. Adaptation by a parasitic trematode to local populations of its snail host. Evolution 43:1663-1671.

Osnas, E.E. and C.M. Lively. 2004. Parasite dose, prevalence of infection and local adaptation in a host-parasite system. Parasitology 128:223-228.

Lively, C.M., M.F. Dybdahl, J. Jokela, E. Osnas, and L.F. Delph. 2004. Host sex and local adaptation by parasites in a snail-trematode interaction. American Naturalist 164:S6-S18.

Koskella, B. and C.M. Lively. 2007. Advice of the Rose: experimental coevolution of a trematode parasite and its snail host. Evolution 62: 152-159.

Koskella, B. and C. M. Lively. 2009. Evidence for negative frequency-dependent selection during experimental coevolution of a freshwater snail and a sterilizing trematode. Evolution 63: 2213-2221.

King, K. C., L. F. Delph, J. Jokela, and C. M. Lively. 2009. The geographic mosaic of sex and the Red Queen. Current Biology 19: 1438–1441.

King, K. C., Delph, L. F., Jokela, J., and Lively, C. M. 2011. Coevolutionary hotspots and coldspots for host sex and parasite local adaptation in a snail-trematode interaction. Oikos 120: 1335-1340.

Morran, L. T., Parrish R. C. II, Gelarden, I. A., Allen, M. B., and Lively, C. M. 2014. Experimental coevolution: rapid local adaptation by parasites depends on host mating system. American Naturalist 184: S91-S100.

Castillo, D.M., Burger, M.K., Lively, C.M., and Delph, L.F. 2015. Experimental evolution: assortative mating and sexual selection, independent of local adaptation, leads to reproductive isolation in the nematode Caenorhabditis remanei. Evolution 69: 3141–3155.

Lively, C.M. 2018. Habitat heterogeneity, host population structure, and parasite local adaptation. Journal of Heredity: 109: 29-37.

Lively. C.M. and M.J. Wade.  2022.  Host-parasite coevolution: partitioning the effects of natural selection and environmental change using coupled Price equations.  Ecology and Evolution 12:e9136.  https://doi.org/10.1002/ece3.9136

Does genetic diversity in host populations hamper the spread of infectious diseases?  If so, does host-parasite coevolution affect the outcome?  We have been studying these questions using mathematical models and synthetic surveys of the literature.

Representative publications

Lively, C.M. and V. Apanius.  1995.  Genetic diversity in host-parasite interactions.  Pp. 421-449 in B.T. Grenfell and A.P. Dobson (eds.), Ecology of Infectious Diseases in Natural Populations.  Cambridge University Press.  Cambridge, U.K.

Agrawal, A. and C.M. Lively. 2002. Infection genetics: gene-for-gene versus matching-allele models, and all points in between. Evolutionary Ecology Research 4:79-90.

Agrawal, A.F. and C.M. Lively. 2003. Modeling infection genetics as a two-step process combining gene-for-gene and matching-allele genetics. Proceedings of the Royal Society, London B. 270:323-334.

Lively, C. M. 2010. The effect of host genetic diversity on disease spread. American Naturalist 175: E149-E152.

King, K. C. and Lively, C. M. 2012. Does genetic diversity limit disease spread in natural host populations? Heredity 109:199-203.

Lively, C. M. 2016.  Coevolutionary epidemiology: disease spread, local adaptation, and sex. American Naturalist 187: E77-E82

Gibson, A.K. and Lively, C.M. 2019. Genetic diversity and disease spread: epidemiological models and empirical studies of a snail-trematode system. Pages 32-57 in K. Wilson, A. Fenton and D. Tomkins (eds.) Wildlife Disease Ecology: Linking Theory to Data and Application. Cambridge University Press.

How are mates chosen?  Are they chosen for traits that are indicative of good genes for parasite resistance or as a way to diversify offspring? How does the mating system affect male mating strategies?  What is the effect of mate choice on reproductive isolation?  

Relevant publications.

Sinervo, B. and C.M. Lively. 1996. The rock-paper-scissors game and the evolution of alternative male strategies. Nature 380: 240-243.

Howard, R. S. and C. M. Lively. 2003. Opposites attract? Mate choice for parasite evasion and the evolutionary stability of sex. Journal of Evolutionary Biology 16:681-689.

Howard, R.S. and C.M. Lively. 2004. Good vs. complementary genes for parasite resistance and the evolution of mate choice. BMC Evolutionary Biology 2004, 4:48

Soper, D. M., Delph, L. F., and Lively, C. M. 2012. Multiple paternity in the freshwater snail, Potamopyrgus antipodarum. Ecology and Evolution 2: 3179-3185.

Dapper, A. L. and Lively, C. M. 2014. Interlocus sexually antagonistic coevolution can create indirect selection for increased recombination. Evolution 68: 1216–1224.

Castillo, D.M., Burger, M.K., Lively, C.M., and Delph, L.F. 2015. Experimental evolution: assortative mating and sexual selection, independent of local adaptation, leads to reproductive isolation in the nematode Caenorhabditis remanei. Evolution 69: 3141–3155.

Lively, C.M. 1986. Canalization versus developmental conversion in a spatially variable environment. American Naturalist 128:561-572

Lively, C.M. 1987. Facultative parthenogenesis and sex-ratio evolution. Evolutionary Ecology 1:297-300

Lively, C.M. 1990. Male allocation and the cost of sex in a parasitic worm. Lectures on Mathematics in the Life Sciences 22:93-107

Lively, C.M. and D.G. Lloyd. 1990. The cost of biparental sex under individual selection. American Naturalist 135:489-500

Lively, C.M. and R.S. Howard. 1994. Selection by parasites for clonal diversity and mixed mating. Philosophical Transactions of the Royal Society 346:271-281.

Lively, C.M. and S.G. Johnson. 1994. Brooding and the evolution of parthenogenesis: strategy models and evidence from aquatic invertebrates. Proceedings of the Royal Society, London B 256:89-95.

Peters, A.D. and C.M. Lively. 1999. The Red Queen and fluctuating epistasis: a population genetic analysis of antagonistic coevolution. American Naturalist 154:393-405

Lively, C.M. 1999. Developmental strategies in spatially variable environments: barnacle shell dimorphism and strategic models of selection. Pages 245-258 in R. Tollrian and C.D. Harvell (eds.), The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton.

Bailey, M., L.F. Delph, and C.M. Lively. 2003. Modeling gynodioecy: novel scenarios for maintaining polymorphism. American Naturalist 161:762-776.

Hazel, W, R. Smock, and C. M. Lively. 2004. The ecological genetics of conditional strategies. American Naturalist 163:888-900.

Lively, C.M, K. Clay, M.J. Wade, and C. Fuqua. 2005. Competitive coexistence in vertically and horizontally transmitted parasites. Evolutionary Ecology Research 7: 1183-1190.

Greischar, M. A. and Lively, C. M. 2011. Parasites can simplify host population dynamics and reduce the risk of extinction. Evolutionary Ecology Research 13:557-569.

Lively, C. M. 2012. Feedbacks between ecology and evolution: interactions between ΔN and Δp in a life-history model. Evolutionary Ecology Research 14: 299-309.