User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Habitat choice meets thermal specialization: Competition with specialists may drive suboptimal habitat preferences in generalists

Primary tabs

Jacob, Staffan [UCL] Laurent, Estelle [UCL] Haegeman, Bart [Station d’Ecologie Théorique et Expérimentale (UMR5321), CNRS, Université Paul Sabatier, F-09200 Moulis, France] Bertrand, Romain [Station d’Ecologie Théorique et Expérimentale (UMR5321), CNRS, Université Paul Sabatier, F-09200 Moulis, France] Prunier, Jérôme G. [Station d’Ecologie Théorique et Expérimentale (UMR5321), CNRS, Université Paul Sabatier, F-09200 Moulis, France] Schtickzelle, Nicolas [UCL]

Limited dispersal is classically considered as a prerequisite for ecological specialization to evolve, such that generalists are expected to show greater dispersal propensity compared with specialists. However, when individuals choose habitats that maximize their performance instead of dispersing randomly, theory predicts dispersal with habitat choice to evolve in specialists, while generalists should disperse more randomly. We tested whether habitat choice is associated with thermal niche specialization using microcosms of the ciliate Tetrahymena thermophila, a species that performs active dispersal. We found that thermal specialists preferred optimal habitats as predicted by theory, a link that should make specialists more likely to track suitable conditions under environmental changes than expected under the random dispersal assumption. Surprisingly, generalists also performed habitat choice but with a preference for suboptimal habitats. Since this result challenges current theory, we developed a metapopulation model to understand under which circumstances such a preference for suboptimal habitats should evolve. We showed that competition between generalists and specialists may favor a preference for niche margins in generalists under environmental variability. Our results demonstrate that the behavioral dimension of dispersal—here, habitat choice—fundamentally alters our predictions of how dispersal evolve with niche specialization, making dispersal behaviors crucial for ecological forecasting facing environmental changes.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès interdit
Publication date 2018
Language Anglais
Journal information "Proceedings of the National academy of sciences of the United States of America" - Vol. 115, no.47, p. 11988-11993 (2018)
Peer reviewed yes
Publisher National academy of sciences
issn 0027-8424
e-issn 1091-6490
Publication status Publié
Affiliation UCL - SST/ELI/ELIB - Biodiversity
Keywords Multidisciplinary
Links
  1. Bolnick Daniel I., Svanbäck Richard, Fordyce James A., Yang Louie H., Davis Jeremy M., Hulsey C. Darrin, Forister Matthew L., The Ecology of Individuals: Incidence and Implications of Individual Specialization, 10.1086/343878
  2. Rainey Paul B., Travisano Michael, 10.1038/27900
  3. Ronce Ophélie, Kirkpatrick Mark, WHEN SOURCES BECOME SINKS: MIGRATIONAL MELTDOWN IN HETEROGENEOUS HABITATS, 10.1111/j.0014-3820.2001.tb00672.x
  4. Kisdi Éva, Dispersal: Risk Spreading versus Local Adaptation, 10.1086/339989
  5. BERG MATTY P., KIERS E. TOBY, DRIESSEN GERARD, van der HEIJDEN MARCEL, KOOI BOB W., KUENEN FRANS, LIEFTING MAARTJE, VERHOEF HERMAN A., ELLERS JACINTHA, Adapt or disperse: understanding species persistence in a changing world, 10.1111/j.1365-2486.2009.02014.x
  6. Buckley Lauren B., Kingsolver Joel G., Functional and Phylogenetic Approaches to Forecasting Species' Responses to Climate Change, 10.1146/annurev-ecolsys-110411-160516
  7. Bonte D., Vandenbroecke N., Lens L., Maelfait J.-P., Low propensity for aerial dispersal in specialist spiders from fragmented landscapes, 10.1098/rspb.2003.2432
  8. Nurmi Tuomas, Parvinen Kalle, On the evolution of specialization with a mechanistic underpinning in structured metapopulations, 10.1016/j.tpb.2007.12.002
  9. Nurmi Tuomas, Parvinen Kalle, Joint evolution of specialization and dispersal in structured metapopulations, 10.1016/j.jtbi.2011.01.023
  10. Lenormand T, Gene flow and the limits to natural selection, 10.1016/s0169-5347(02)02497-7
  11. Kawecki Tadeusz J., Ebert Dieter, Conceptual issues in local adaptation, 10.1111/j.1461-0248.2004.00684.x
  12. Jocque Merlijn, Field Richard, Brendonck Luc, De Meester Luc, Climatic control of dispersal-ecological specialization trade-offs: a metacommunity process at the heart of the latitudinal diversity gradient? : Climate, dispersal, ecological specialization and diversity, 10.1111/j.1466-8238.2009.00510.x
  13. Bolnick Daniel I., Nosil Patrik, NATURAL SELECTION IN POPULATIONS SUBJECT TO A MIGRATION LOAD, 10.1111/j.1558-5646.2007.00179.x
  14. Stevens Virginie M., Whitmee Sarah, Le Galliard Jean-François, Clobert Jean, Böhning-Gaese Katrin, Bonte Dries, Brändle Martin, Matthias Dehling D., Hof Christian, Trochet Audrey, Baguette Michel, A comparative analysis of dispersal syndromes in terrestrial and semi-terrestrial animals, 10.1111/ele.12303
  15. Dahirel Maxime, Olivier Eric, Guiller Annie, Martin Marie-Claire, Madec Luc, Ansart Armelle, Movement propensity and ability correlate with ecological specialization in European land snails: comparative analysis of a dispersal syndrome, 10.1111/1365-2656.12276
  16. Clavel Joanne, Julliard Romain, Devictor Vincent, Worldwide decline of specialist species: toward a global functional homogenization?, 10.1890/080216
  17. Jarzyna Marta A., Porter William F., Maurer Brian A., Zuckerberg Benjamin, Finley Andrew O., Landscape fragmentation affects responses of avian communities to climate change, 10.1111/gcb.12885
  18. Bowler Diana E., Benton Tim G., Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics, 10.1017/s1464793104006645
  19. Ronce Ophélie, How Does It Feel to Be Like a Rolling Stone? Ten Questions About Dispersal Evolution, 10.1146/annurev.ecolsys.38.091206.095611
  20. Holt Robert D., Population dynamics and evolutionary processes: the manifold roles of habitat selection, 10.1007/bf02071557
  21. Edelaar Pim, Siepielski Adam M., Clobert Jean, MATCHING HABITAT CHOICE CAUSES DIRECTED GENE FLOW: A NEGLECTED DIMENSION IN EVOLUTION AND ECOLOGY, 10.1111/j.1558-5646.2008.00459.x
  22. Jacob Staffan, Bestion Elvire, Legrand Delphine, Clobert Jean, Cote Julien, Habitat matching and spatial heterogeneity of phenotypes: implications for metapopulation and metacommunity functioning, 10.1007/s10682-015-9776-5
  23. Travis Justin M. J., Delgado Maria, Bocedi Greta, Baguette Michel, Bartoń Kamil, Bonte Dries, Boulangeat Isabelle, Hodgson Jenny A., Kubisch Alexander, Penteriani Vincenzo, Saastamoinen Marjo, Stevens Virginie M., Bullock James M., Dispersal and species’ responses to climate change, 10.1111/j.1600-0706.2013.00399.x
  24. Jacob Staffan, Legrand Delphine, Chaine Alexis S., Bonte Dries, Schtickzelle Nicolas, Huet Michèle, Clobert Jean, Gene flow favours local adaptation under habitat choice in ciliate microcosms, 10.1038/s41559-017-0269-5
  25. Holt Robert D., Barfield Michael, Habitat Selection and Niche Conservatism, 10.1560/ijee.54.3-4.295
  26. Holt, Evol Ecol Res, 5, 159 (2003)
  27. Mortier Frederik, Jacob Staffan, Vandegehuchte Martijn L., Bonte Dries, Habitat choice stabilizes metapopulation dynamics through increased ecological specialisation., 10.1101/267575
  28. Rosenzweig Michael L., Habitat selection as a source of biological diversity, 10.1007/bf02071556
  29. Brown Joel S., Pavlovic Noel B., Evolution in heterogeneous environments: Effects of migration on habitat specialization, 10.1007/bf02270698
  30. Jessup Christine M., Kassen Rees, Forde Samantha E., Kerr Ben, Buckling Angus, Rainey Paul B., Bohannan Brendan J.M., Big questions, small worlds: microbial model systems in ecology, 10.1016/j.tree.2004.01.008
  31. Altermatt Florian, Fronhofer Emanuel A., Garnier Aurélie, Giometto Andrea, Hammes Frederik, Klecka Jan, Legrand Delphine, Mächler Elvira, Massie Thomas M., Pennekamp Frank, Plebani Marco, Pontarp Mikael, Schtickzelle Nicolas, Thuillier Virginie, Petchey Owen L., Big answers from small worlds: a user's guide for protist microcosms as a model system in ecology and evolution, 10.1111/2041-210x.12312
  32. Bestion Elvire, Clobert Jean, Cote Julien, Dispersal response to climate change: scaling down to intraspecific variation, 10.1111/ele.12502
  33. Clobert Jean, Le Galliard Jean-François, Cote Julien, Meylan Sandrine, Massot Manuel, Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations, 10.1111/j.1461-0248.2008.01267.x
  34. Bertrand Romain, Riofrío-Dillon Gabriela, Lenoir Jonathan, Drapier Jacques, de Ruffray Patrice, Gégout Jean-Claude, Loreau Michel, Ecological constraints increase the climatic debt in forests, 10.1038/ncomms12643
  35. Ravigné Virginie, Dieckmann Ulf, Olivieri Isabelle, Live Where You Thrive: Joint Evolution of Habitat Choice and Local Adaptation Facilitates Specialization and Promotes Diversity, 10.1086/605369
  36. Edelaar Pim, Bolnick Daniel I., Non-random gene flow: an underappreciated force in evolution and ecology, 10.1016/j.tree.2012.07.009
  37. Scheiner Samuel M., Habitat Choice and Temporal Variation Alter the Balance between Adaptation by Genetic Differentiation, a Jack-of-All-Trades Strategy, and Phenotypic Plasticity, 10.1086/685812
  38. Edelaar Pim, Jovani Roger, Gomez-Mestre Ivan, Should I Change or Should I Go? Phenotypic Plasticity and Matching Habitat Choice in the Adaptation to Environmental Heterogeneity, 10.1086/693345
  39. Schmidt Kenneth A., Earnhardt Joanne M., Brown Joel S., Holt Robert D., HABITAT SELECTION UNDER TEMPORAL HETEROGENEITY: EXORCIZING THE GHOST OF COMPETITION PAST, 10.1890/0012-9658(2000)081[2622:hsuthe]2.0.co;2
  40. Abrams Peter A., The Prerequisites for and Likelihood of Generalist‐Specialist Coexistence, 10.1086/499382
  41. Bohn Thomas, Amundsen Per-Arne, The Competitive Edge of an Invading Specialist, 10.2307/2680222
  42. Wolf Jason B., Brodie III Edmund D., Moore Allen J., Interacting Phenotypes and the Evolutionary Process. II. Selection Resulting from Social Interactions, 10.1086/303168
  43. Abrams Peter A., Implications of flexible foraging for interspecific interactions: lessons from simple models, 10.1111/j.1365-2435.2009.01621.x
  44. Rahmstorf S., Coumou D., Increase of extreme events in a warming world, 10.1073/pnas.1101766108
  45. Hendry Andrew P., Eco-evolutionary Dynamics, ISBN:9781400883080, 10.1515/9781400883080
  46. Coumou Dim, Rahmstorf Stefan, A decade of weather extremes, 10.1038/nclimate1452
  47. Binckley Christopher A., Resetarits William J., Habitat selection determines abundance, richness and species composition of beetles in aquatic communities, 10.1098/rsbl.2005.0310
  48. Resetarits William J., Binckley Christopher A., Spatial contagion of predation risk affects colonization dynamics in experimental aquatic landscapes, 10.1890/08-0613.1
  49. Akcali Christopher K., Porter Cody K., Comment on Van Belleghem et al. 2016: Habitat choice mechanisms in speciation and other forms of diversification : HABITAT CHOICE MECHANISMS, 10.1111/evo.13375
  50. Jaenike John, Holt Robert D., Genetic Variation for Habitat Preference: Evidence and Explanations, 10.1086/285140
  51. Legrand Delphine, Trochet Audrey, Moulherat Sylvain, Calvez Olivier, Stevens Virginie M., Ducatez Simon, Clobert Jean, Baguette Michel, Ranking the ecological causes of dispersal in a butterfly, 10.1111/ecog.01283
  52. Jacob Staffan, Chaine Alexis S., Schtickzelle Nicolas, Huet Michèle, Clobert Jean, Social information from immigrants: multiple immigrant-based sources of information for dispersal decisions in a ciliate, 10.1111/1365-2656.12380
  53. Pennekamp, PeerJ Prepr, 6, e26540v1 (2018)
  54. Pennekamp, Evolution, 68, 2319 (2014)
  55. Jacob Staffan, Clobert Jean, Legrand Delphine, Schtickzelle Nicolas, Chaine Alexis S., Social Information in Cooperation and Dispersal in Tetrahymena, Biocommunication of Ciliates (2016) ISBN:9783319322094 p.235-252, 10.1007/978-3-319-32211-7_14
  56. MacLean Sarah A., Beissinger Steven R., Species’ traits as predictors of range shifts under contemporary climate change: A review and meta-analysis, 10.1111/gcb.13736
  57. DALL S, GIRALDEAU L, OLSSON O, MCNAMARA J, STEPHENS D, Information and its use by animals in evolutionary ecology, 10.1016/j.tree.2005.01.010
  58. Miner Benjamin G., Sultan Sonia E., Morgan Steven G., Padilla Dianna K., Relyea Rick A., Ecological consequences of phenotypic plasticity, 10.1016/j.tree.2005.08.002
  59. Violle Cyrille, Enquist Brian J., McGill Brian J., Jiang Lin, Albert Cécile H., Hulshof Catherine, Jung Vincent, Messier Julie, The return of the variance: intraspecific variability in community ecology, 10.1016/j.tree.2011.11.014
  60. Gibert Jean P., Dell Anthony I., DeLong John P., Pawar Samraat, Scaling-up Trait Variation from Individuals to Ecosystems, Trait-Based Ecology - From Structure to Function (2015) ISBN:9780128024454 p.1-17, 10.1016/bs.aecr.2015.03.001
  61. Legrand Delphine, Cote Julien, Fronhofer Emanuel A., Holt Robert D., Ronce Ophélie, Schtickzelle Nicolas, Travis Justin M. J., Clobert Jean, Eco-evolutionary dynamics in fragmented landscapes, 10.1111/ecog.02537
  62. Collins K (2012) Tetrahymena Thermophila (Elsevier, New York).
  63. Zufall Rebecca A., Dimond Kristen L., Doerder F. Paul, Restricted distribution and limited gene flow in the model ciliateTetrahymena thermophila, 10.1111/mec.12066
  64. Pennekamp F (2014) Swiming with ciliates—dispersal and movement ecology of Tetrahymena thermophila. PhD dissertation (Université Catholique de Louvain, Louvain-la-Neuve, Belgium).
  65. Hastie Trevor, Tibshirani Robert, Generalized Additive Models, 10.1214/ss/1177013604
  66. Oksanen Jari, Minchin Peter R, Continuum theory revisited: what shape are species responses along ecological gradients?, 10.1016/s0304-3800(02)00190-4
  67. Cote Julien, Bestion Elvire, Jacob Staffan, Travis Justin, Legrand Delphine, Baguette Michel, Evolution of dispersal strategies and dispersal syndromes in fragmented landscapes, 10.1111/ecog.02538
  68. Bertrand Romain, Gégout Jean-Claude, Bontemps Jean-Daniel, Niches of temperate tree species converge towards nutrient-richer conditions over ontogeny, 10.1111/j.1600-0706.2011.19582.x
  69. Chaine, Evolution, 64, 1290 (2010)
  70. Schtickzelle Nicolas, Fjerdingstad Else J, Chaine Alexis, Clobert Jean, Cooperative social clusters are not destroyed by dispersal in a ciliate, 10.1186/1471-2148-9-251
  71. Pennekamp Frank, Schtickzelle Nicolas, Implementing image analysis in laboratory-based experimental systems for ecology and evolution: a hands-on guide, 10.1111/2041-210x.12036
  72. Jacob Staffan, Wehi Priscilla, Clobert Jean, Legrand Delphine, Schtickzelle Nicolas, Huet Michele, Chaine Alexis, Cooperation-mediated plasticity in dispersal and colonization : COOPERATION AND THE PLASTICITY OF DISPERSAL, 10.1111/evo.13028
  73. Nimon Kim, Lewis Mitzi, Kane Richard, Haynes R. Michael, An R package to compute commonality coefficients in the multiple regression case: An introduction to the package and a practical example, 10.3758/brm.40.2.457
  74. Ray-Mukherjee Jayanti, Nimon Kim, Mukherjee Shomen, Morris Douglas W., Slotow Rob, Hamer Michelle, Using commonality analysis in multiple regressions: a tool to decompose regression effects in the face of multicollinearity, 10.1111/2041-210x.12166
  75. Egas Martijn, Dieckmann Ulf, Sabelis Maurice W., Evolution Restricts the Coexistence of Specialists and Generalists: The Role of Trade‐off Structure, 10.1086/382599
  76. Loreau M., Mouquet N., Gonzalez A., Biodiversity as spatial insurance in heterogeneous landscapes, 10.1073/pnas.2235465100
  77. Dispersal Ecology and Evolution, ISBN:9780199608898, 10.1093/acprof:oso/9780199608898.001.0001
Bibliographic reference Jacob, Staffan ; Laurent, Estelle ; Haegeman, Bart ; Bertrand, Romain ; Prunier, Jérôme G. ; et. al. Habitat choice meets thermal specialization: Competition with specialists may drive suboptimal habitat preferences in generalists. In: Proceedings of the National academy of sciences of the United States of America, Vol. 115, no.47, p. 11988-11993 (2018)
Permanent URL http://hdl.handle.net/2078.1/208623