The balance between risk and benefit of exploiting resources drives life-history evolution in organisms. Predators are naturally recognized as major drivers of the life-history evolution of their prey. Although prey may also influence the life-history evolution of their predators in the context of an evolutionary arms race, there is far more evidence of the role of predators than of prey.The goal of this study was to investigate the role of prey in life-history evolution of predators using ladybird beetle predators of aphids and coccids. These particular ladybirds and their prey were chosen because literature shows that the pace of life of aphids is faster than that of coccids and this difference is reflected in the life histories of the ladybirds that specialize on feeding on aphids or coccids.Thirty-four species of ladybird predators of aphids and eight of coccids belonging to five different tribes were collected and reared in the laboratory. The females were weighed as well as their eggs, and their reproductive investment estimated as the number of ovarioles. Phylogenetic relatedness was controlled for in the statistical analyses.Controlling for female mass revealed that ladybird predators of aphids lay bigger eggs than ladybird predators of coccids. This difference is not influenced by phylogenetic relatedness but only by the type of prey eaten. We suggest that ladybird predators of coccids lay smaller eggs because neonate larvae do not have to search, catch, and subdue prey. Both types of ladybirds have a similar reproductive investment relative to their body mass when phylogeny is controlled for.Recognizing the influence of prey on the life-history evolution of predators is important for understanding food web dynamics. From an applied perspective, this fine evolutionary tuning of prey-predator relationships should be used to guide and increase the efficiency of biological control programs.

Global Change Research Institute CAS Brno Czech Republic

INRAE Aix Marseille University UMR RECOVER Aix en Provence France

Laboratoire Évolution and Diversité Biologique Université de Toulouse CNRS IRD UPS Toulouse France

School of Biological Sciences University of East Anglia Norwich UK

Zobrazit více v PubMed

Abrams, P. A. (2001). Predator‐prey interactions. In Fox C. W., Roff D. A., & Fairbairn D. J. (Eds.), Evolutionary ecology. Concepts and case studies (pp. 277–289). Oxford University Press.

Agrawal, A. A. (2007). Macroevolution of plant defence strategies. Trends in Ecology & Evolution, 22, 103–109. 10.1016/j.tree.2006.10.012 PubMed DOI

Albuquerque, G. S. , Tauber, M. J. , & Tauber, C. A. (1997). Life‐history adaptations and reproductive costs associated with specialization in predacious insects. The Journal of Animal Ecology, 66(3), 307–317. 10.2307/5977 DOI

Bhat, U. , Kempes, C. P. , & Yeakel, J. D. (2020). Scaling the risk landscape drives optimal life‐history strategies and the evolution of grazing. Proceedings of the National Academy of Sciences, 117(3), 1580–1586. 10.1073/pnas.1907998117 PubMed DOI PMC

Borges, I. , Soares, A. O. , Magro, A. , & Hemptinne, J.‐L. (2011). Prey availability in time and space is a driving force in life history evolution of predatory insects. Evolutionary Ecology, 25(6), 1307–1319. 10.1007/s10682-011-9481-y DOI

Brown, J. H. , Gillooly, J. F. , Allen, A. P. , Savage, V. M. , & West, G. B. (2004). Toward a metabolic theory of ecology. Ecology, 85(7), 1771–1789. 10.1890/03-9000 DOI

Burger, J. R. , Hou, C. , & Brown, J. H. (2019). Toward a metabolic theory of life history. Proceedings of the National Academy of Sciences, 116(52), 26653–26661. 10.1073/pnas.1907702116 PubMed DOI PMC

Bursell, E. (1970). An introduction to insect physiology. Academic Press.

Canard, M. (2001). Natural food and feeding habits of lacewings. In McEwen P., New T., & Whittington A. (Eds.), Lacewings in the crop environment (pp. 116–130). Cambridge University Press.

Chapman, R. F. (1998). The insects: structure and function. Cambridge University Press.

Che, L. , Zhang, P. , Deng, S. , Escalona, H. E. , Wang, X. , Li, Y. , Pang, H. , Vandenberg, N. , Slipinski, A. , Tomaszewska, W. , & Liang, D. (2021). New insights into the phylogeny and evolution of Lady Beetles (Coleoptera: Coccinellidae) by extensive sampling of genes and species. Molecular Phylogenetics and Evolution, 156, 107045. 10.1016/j.ympev.2020.107045 PubMed DOI

Church, S. H. , de Medeiros, B. A. S. , Donoughe, S. , Márquez Reyes, N. L. , & Extavour, C. G. (2021). Repeated loss of variation in insect ovary morphology s the role of development in life‐history evolution. Proceedings of the Royal Society B: Biological Sciences, 288(1950), 20210150. 10.1098/rspb.2021.0150 PubMed DOI PMC

Cini, A. , Meconcelli, S. , & Cervo, R. (2013). Ovarian indexes as indicators of reproductive investment and egg‐laying activity in social insects: A comparison among methods. Insectes Sociaux, 60(3), 393–402. 10.1007/s00040-013-0305-7 DOI

Clissold, F. J. , & Simpson, S. J. (2015). Temperature, food quality and life history traits of herbivorous insects. Current Opinion in Insect Science, 11, 63–70. 10.1016/j.cois.2015.10.011 PubMed DOI

Cott, H. B. (1940). Adaptive coloration in animals. Methuen.

Dixon, A. F. G. (1958). Escape responses shown by certain aphids to the presence of the coccinellid, Adalia decempunctata (L.). Transactions of the Royal Entomological Society of London, 10, 319–334. 10.1111/j.1365-2311.1958.tb00786.x DOI

Dixon, A. F. G. (1959). An experimental study of the searching behaviour of the predatory beetle Adalia decempunctata (L.). Journal of Animal Ecology, 35, 105–112. 10.2307/2082 DOI

Dixon, A. F. G. (1998). Aphid ecology. An optimization approach (2nd ed.). Chapman & Hall.

Dixon, A. F. G. (2000). Insect predator‐prey dynamics. Ladybird beetles and biological control. Cambridge University Press.

Dixon, A. F. G. (2015). Pace of life of insect natural enemies. Acta Societatis Zoologicae Bohemicae, 79, 45–50.

Dixon, A. F. G. , & Agarwala, B. K. (1999). Ladybird‐induced life–history changes in aphids. Proceedings of the Royal Society of London. Series B: Biological Sciences, 266(1428), 1549–1553. 10.1098/rspb.1999.0814 DOI

Dixon, A. F. G. , Agarwala, B. K. , Hemptinne, J.‐L. , Honek, A. , & Jarosik, V. (2011). Fast‐slow continuum in the life‐history parameters of ladybirds revisited. European Journal of Environmental Sciences, 1, 61–66. 10.14712/23361964.2015.67 DOI

Dixon, A. F. G. , & Hemptinne, J.‐L. (2001). Body size distribution in predatory ladybird beetles reflects that of their prey. Ecology, 82, 1847–1856.

Dixon, A. F. G. , Hemptinne, J.‐L. , & Kindlmann, P. (1997). Effectiveness of ladybirds as biological control agents: Patterns and processes. Entomophaga, 42, 71–83. 10.1007/BF02769882 DOI

Dixon, A. F. G. , & Honek, A. (2014). Rate of development of predatory insects is dependent on that of their prey. European Journal of Environmental Sciences, 4, 87–91. 10.14712/23361964.2014.1 DOI

Dixon, A. F. G. , Kindlmann, P. , Leps, J. , & Holman, J. (1987). Why are there so few species of aphids, especially in the tropics. The American Naturalist, 129, 580–592. 10.1086/284659 DOI

Dixon, A. F. G. , Sato, S. , & Kindlmann, P. (2016). Evolution of slow and fast development in predatory ladybirds. Journal of Applied Entomology, 140, 103–114. 10.1111/jen.12221 DOI

Douglas, A. E. (2003). Nutritional physiology of aphids. Advances in Insect Physiology, 31, 73–140. 10.1016/S0065-2806(03)31002-1 DOI

Dziock, F. (2005). Evolution of prey specialization in aphidophagous syrphids of the genera Melanostoma and Platycheirus (Diptera: Syrphidae) 1. Body size, development, and prey traits. European Journal of Entomology, 102, 413–421. 10.14411/eje.2005.059 DOI

Erb, M. , & Robert, C. A. M. (2016). Sequestration of plant secondary metabolites by insect herbivores: Molecular mechanisms and ecological consequences. Current Opinion in Insect Science, 14, 8–11. 10.1016/j.cois.2015.11.005 PubMed DOI

Escalona, H. E. , Zwick, A. , Li, H.‐S. , Li, J. , Wang, X. , Pang, H. , Hartley, D. , Jermijn, L. S. , Nedved, O. , Misof, B. , Niehuis, O. , Slipinski, A. , & Tomaszewska, W. (2017). Molecular phylogeny reveals food plasticity in the evolution of true ladybird beetles (Coleoptera: Coccinellidae: Coccinellini). BMC Evolutionary Biology, 17(1), 151. 10.1186/s12862-017-1002-3 PubMed DOI PMC

Frechette, B. , Alauzet, C. , & Hemptinne, J.‐L. (2003). Oviposition behaviour of the two‐spot ladybird beetle Adalia bipunctata (l.) (Coleoptera: Coccinellidae) on plants with conspecific larval tracks. In Biology, Ecology and Behaviour of Aphidophagous Insects. Proc. 8th Int. Symp. Ecology of Aphidophaga. Arquipelago. Life and Marine Sciences. Supplement (Vol. 5, pp. 73–77).

Giorgi, J. A. , Vandenberg, N. J. , McHugh, J. V. , Forrester, J. A. , Ślipiński, S. A. , Miller, K. B. , Shapiro, L. R. , & Whiting, M. F. (2009). The evolution of food preferences in Coccinellidae. Biological Control, 51(2), 215–231. 10.1016/j.biocontrol.2009.05.019 DOI

Glendinning, J. I. (2007). How do predators cope with chemically defended foods? The Biological Bulletin, 213, 252–266. 10.2307/25066643 PubMed DOI

Guindon, S. , & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704. 10.1080/10635150390235520 PubMed DOI

Hartbauer, M. (2010). Collective defense of Aphis nerii and Uroleucon hypochoeridis (Homoptera, Aphididae) against natural enemies. PLoS One, 5, e10417. 10.1371/journal.pone.0010417 PubMed DOI PMC

Heimpel, G. E. , & Mills, N. J. (2017). Biological control. Ecology and applications. Cambridge University Press.

Hemptinne, J.‐L. , Dixon, A. F. G. , & Coffin, J. (1992). Attack strategy of ladybird beetles (Coccinellidae): Factors shaping their numerical response. Oecologia, 90, 238–245. 10.1007/BF00317181 PubMed DOI

Herz, A. , & Heitland, W. (2002). Comparison of the fat allocation patterns in female pine sawflies (Hymenoptera: Diprionidae). European Journal of Entomology, 99(1), 117–120. 10.14411/eje.2002.020 DOI

Hironori, Y. , & Katsuhiro, S. (1997). Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga, 42, 153–163. 10.1007/BF02769893 DOI

Hodek, I. (1973). Biology of Coccinellidae. Dr. W. Junk N. V. Publishers & Academia Publishing House of the Czechoslovak Academy of Sciences.

Hodek, I. , van Emden, H. F. , & Honek, A. (2012). Ecology and behaviour of the ladybird beetles (Coccinellidae). Wiley‐Blackwell.

Ioannou, C. C. , Bartumeus, F. , Krause, J. , & Ruxton, G. D. (2011). Unified effects of aggregation reveal larger prey groups take longer to find. Proceedings of the Royal Society B: Biological Sciences, 278(1720), 2985–2990. 10.1098/rspb.2011.0003 PubMed DOI PMC

Jarvis, K. J. , Haas, F. , & Whiting, M. F. (2004). Phylogeny of earwigs (Insecta: Dermaptera) based on molecular and morphological evidence: reconsidering the classification of Dermaptera. Systematic Entomology, 30, 1–12. 10.1111/j.1365-3113.2004.00276.x DOI

Johnson, K. P. , Dietrich, C. H. , Friedrich, F. , Beutel, R. G. , Wipfler, B. , Peters, R. S. , Allen, J. M. , Petersen, M. , Donath, A. , Walden, K. K. O. , Kozlov, A. M. , Podsiadlowski, L. , Mayer, C. , Meusemann, K. , Vasilikopoulos, A. , Waterhouse, R. M. , Cameron, S. L. , Weirauch, C. , Swanson, D. R. , & Yoshizawa, K. (2018). Phylogenomics and the evolution of hemipteroid insects. Proceedings of the National Academy of Sciences, 115(50), 12775–12780. 10.1073/pnas.1815820115 PubMed DOI PMC

Karley, A. J. , Parker, W. E. , Pitchford, J. W. , & Douglas, A. E. (2004). The mid‐season crash in aphid populations: Why and how does it occur? Ecological Entomology, 29, 383–388. 10.1111/j.0307-6946.2004.00624.x DOI

Katoh, K. , & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. 10.1093/molbev/mst010 PubMed DOI PMC

Kindlmann, P. , & Dixon, A. F. G. (1999). Generation time ratios – Determinants of prey abundance in insect predator‐prey interactions. Biological Control, 16, 133–138. 10.1006/bcon.1999.0754 DOI

Kindlmann, P. , Štípková, Z. , & Dixon, A. F. G. (2021). Generation time ratio, rather than voracity, determines population dynamics of insect – Natural enemy systems, contrary to classical Lotka‐Volterra models. European Journal of Environmental Sciences, 10(2), 133–140. 10.14712/23361964.2020.15 DOI

Kramer, D. L. (2001). Foraging behavior. In Fox C. W., Roff D. A., & Fairbairn D. A. (Eds.), Evolutionary ecology. Concepts and case studies (pp. 232–246). Oxford University Press.

Laughlin, D. C. , Gremer, J. R. , Adler, P. B. , Mitchell, R. M. , & Moore, M. M. (2020). The Net Effect of Functional Traits on Fitness. Trends in Ecology & Evolution, 35(11), 1037–1047. 10.1016/j.tree.2020.07.010 PubMed DOI

Law, R. (1979). Optimal life histories under age‐specific predation. The American Naturalist, 114, 399–417. 10.1086/283488 DOI

Lefort, V. , Longueville, J. E. , & Gascuel, O. (2017). SMS: Smart model selection in PhyML. Molecular Biology and Evolution, 34, 2422–2424. 10.1093/molbev/msx149 PubMed DOI PMC

Litsios, G. , & Salamin, N. (2012). Effects of phylogenetic signal on ancestral state reconstruction. Systematic Biology, 61, 533–538. 10.1093/sysbio/syr124 PubMed DOI

Magro, A. , Hemptinne, J.‐L. , Navarre, A. , & Dixon, A. F. G. (2003). Comparison of the reproductive investment in Coccidophagous and Aphidophagous ladybirds (Coleoptera: Coccinellidae). Archipélago – Life and Marine Sciences, Supplement 5, 29–31.

Magro, A. , Lecompte, E. , Magné, F. , Hemptinne, J.‐L. , & Crouau‐Roy, B. (2010). Phylogeny of ladybirds (Coleoptera: Coccinellidae): Are the subfamilies monophyletic? Molecular Phylogenetics and Evolution, 54, 833–848. 10.1016/j.ympev.2009.10.022 PubMed DOI

Majerus, M. E. N. , Sloggett, J. J. , Godeau, J.‐F. , & Hemptinne, J.‐L. (2007). Interactions between ants and aphidophagous and coccidophagous ladybirds. Population Ecology, 49(1), 15–27. 10.1007/s10144-006-0021-5 DOI

Merlin, J. , Lemaître, O. , & Grégoire, J.‐C. (1996). Chemical cues produced by conspecific larvae deter oviposition by the coccidophagous ladybird beetle, Cryptolaemus montrouzieri . Entomologia Experimentalis Et Applicata, 79, 147–151. 10.1111/j.1570-7458.1996.tb00820.x DOI

Miller, G. L. , Oswald, J. D. , & Miller, D. R. (2004). Lacewings and scale insects: A review of predator/prey associations between the Neuropteridae and Coccoidea (Insecta: Neuroptera, Raphidioptera, Hemiptera). Annals of the Entomological Society of America, 97, 1103–1125.

Mills, N. J. (2018). An alternative perspective for the theory of biological control. Insects, 9, 131. 10.3390/insects9040131 PubMed DOI PMC

Molina‐Venegas, R. , & Rodríguez, M. A. (2017). Revisiting phylogenetic signal; strong or negligible impacts of polytomies and branch length information? BMC Evolutionary Biology, 17, 53. 10.1186/s12862-017-0898-y PubMed DOI PMC

Münkemüller, T. , Lavergne, S. , Bzeznik, B. , Dray, S. , Jombart, T. , Schiffers, K. , & Thuiller, W. (2012). How to measure and test phylogenetic signal. Methods in Ecology and Evolution, 3, 743–576. 10.1111/j.2041-210X.2012.00196.x DOI

Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature, 401, 877–884. 10.1038/44766 PubMed DOI

Ponsonby, D. J. , & Copland, M. J. W. (1998). Environmental influences on fecundity, egg viability and egg cannibalism in the scale insect predator, Chilocorus nigritus . BioControl, 43, 39–52. 10.1023/A:1009928305305 DOI

R Core Team . (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R‐project.org/

Rana, J. S. , Dixon, A. F. G. , & Jarosik, V. (2002). Costs and benefits of prey specialization in a generalist insect predator. Journal of Animal Ecology, 71, 15–22. 10.1046/j.0021-8790.2001.00574.x DOI

Reznick, D. A. , Bryga, H. , & Endler, J. A. (1990). Experimentally induced life‐history evolution in a natural population. Nature, 346, 357–359. 10.1038/346357a0 DOI

Robertson, J. A. , Ślipiński, A. , Moulton, M. , Shockley, F. W. , Giorgi, A. , Lord, N. P. , Mckenna, D. D. , Tomaszewska, W. , Forrester, J. , Miller, K. B. , Whiting, M. F. , & Mchugh, J. V. (2015). Phylogeny and classification of Cucujoidea and the recognition of a new Superfamily Coccinelloidea (Coleoptera: Cucujiformia). Systematic Entomology, 40, 745–778. 10.1111/syen.12138 DOI

Robertson, J. A. , Whiting, M. F. , & McHugh, J. V. (2008). Searching for natural lineages within the Cerylonid Series (Coleoptera: Cucujoidea). Molecular Phylogenetics and Evolution, 46, 193–205. 10.1016/j.ympev.2007.09.017 PubMed DOI

Roff, D. A. (2002). Life history evolution. Sinauer Associates Inc.

Ronquist, F. , & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574. 10.1093/bioinformatics/btg180 PubMed DOI

Scott, R. , MacPherson, B. , & Gras, R. (2018). A comparison of stable and fluctuating resources with respect to evolutionary adaptation and life history traits using individual‐based modelling and machine learning. Journal of Theoretical Biology, 459, 52–66. 10.1016/j.jtbi.2018.09.019 PubMed DOI

Seago, A. E. , Giorgi, J. A. , Li, J. , & Ślipiński, A. (2011). Phylogeny, classification and evolution of ladybird beetles (Coleoptera: Coccinellidae) based on simultaneous analysis of molecular and morphological data. Molecular Phylogenetics and Evolution, 60(1), 137–151. 10.1016/j.ympev.2011.03.015 PubMed DOI

Sentis, A. , Bertram, R. , Dardenne, N. , Ramon‐Portugal, F. , Espinasse, G. , Louit, I. , Negri, L. , Haeler, E. , Ashkar, T. , Pannetier, T. , Cunningham, J. L. , Grunau, C. , Le Trionnaire, G. , Simon, J.‐C. , Magro, A. , Pujol, B. , Hemptinne, J.‐L. , & Danchin, E. (2018). Evolution without standing genetic variation: Change in transgenerational plastic response under persistent predation pressure. Heredity, 121, 266–281. 10.1038/s41437-018-0108-8 PubMed DOI PMC

Sentis, A. , Lucas, E. , & Vickery, W. L. (2012). Prey abundance, intraguild predators, ants and the optimal egg‐laying strategy of a furtive predator. Journal of Insect Behavior, 25, 529–542. 10.1007/s10905-012-9320-1 DOI

Song, N. , Zhang, H. , & Zhao, T. (2019). Insights into the phylogeny of Hemiptera from increased mitogenomic taxon sampling. Molecular Phylogenetics and Evolution, 137, 236–249. 10.1016/j.ympev.2019.05.009f PubMed DOI

Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post‐analysis of large phylogenies. Bioinformatics, 30, 1312–1313. 10.1093/bioinformatics/btu033 PubMed DOI PMC

Stearns, S. C. (1992). The evolution of life histories. Oxford University Press.

Stewart, L. A. , Hemptinne, J.‐L. , & Dixon, A. F. G. (1991). Reproductive tactics of ladybird beetles: Relationships between egg size, ovariole number and developmental time. Functional Ecology, 5(3), 380–385. 10.2307/2389809 DOI

Symonds, M. R. E. , & Blomberg, S. P. (2014). A primer on phylogenetic generalised least squares. In Garamszegi L. Z. (Ed.), Modern phylogenetic comparative methods and their application in evolutionary biology (pp. 105–130). Springer.

Taylor, R. J. (1977). The value of clumping to prey. Experiments with a mammalian predator. Oecologia, 30, 285–294. 10.1007/BF01833636 PubMed DOI

Ugine, T. A. , Krasnoff, S. B. , Grebenok, R. J. , Behmer, S. T. , & Losey, J. E. (2018). Prey nutrient content creates omnivores out of predators. Ecology Letters, 275–283. 10.1111/ele.13186 PubMed DOI

Vandenberg, N. J. (2002). Coccinellidae. In Arnett R. H., Thomas M. C. Jr, Skelley P. E., & Frank J. H. (Eds.), American beetles (pp. 371–389). CRC Press.

Vantaux, A. , Roux, O. , Magro, A. , & Orivel, J. (2012). Evolutionary perspectives on myrmecophily in ladybirds. Psyche, 2012, e591570. 10.1155/2012/591570 DOI

Wheeler, D. (1996). The role of nourishment in oogenesis. Annual Review of Entomology, 41, 407–431. 10.1146/annurev.en.41.010196.002203 PubMed DOI

Whiting, M. F. (2002). Mecoptera is paraphyletic: Multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta, 31, 93–104. 10.1046/j.0300-3256.2001.00095.x DOI

Wilson, A. M. , Hubel, T. A. , Wilshin, S. D. , Lowe, J. C. , Lorenc, M. , Dewhirst, O. P. , Bartlam‐Brooks, H. L. A. , Diack, R. , Bennitt, E. , Golabek, K. A. , Woledge, R. C. , McNutt, J. W. , Curtin, N. A. , & West, T. G. (2018). Biomechanics of predator‐prey arms race in Lion, Zebra, Cheetah and Impala. Nature, 554, 183–188. 10.1038/nature25479 PubMed DOI

Wu, G.‐M. , Boivin, G. , Brodeur, J. , Giraldeau, L.‐A. , & Outreman, Y. (2010). Altruistic defence behaviours in aphids. BMC Evolutionary Biology, 10(1), 19. 10.1186/1471-2148-10-19 PubMed DOI PMC

Zwickl, D. J. (2006). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. The University of Texas (USA). PhD Thesis.

Ecological consequences of body size reduction under warming

Zobrazit více v PubMed

Dryad
10.5061/dryad.pg4f4qrqz