Mutualisms in a changing world: an evolutionary perspective.

Ecology Letters (2010) 13: 1459-1474 ABSTRACT: There is growing concern that rapid environmental degradation threatens mutualistic interactions. Because mutualisms can bind species to a common fate, mutualism breakdown has the potential to expand and accelerate effects of global change on biodiversity loss and ecosystem disruption. The current focus on the ecological dynamics of mutualism under global change has skirted fundamental evolutionary issues. Here, we develop an evolutionary perspective on mutualism breakdown to complement the ecological perspective, by focusing on three processes: (1) shifts from mutualism to antagonism, (2) switches to novel partners and (3) mutualism abandonment. We then identify the evolutionary factors that may make particular classes of mutualisms especially susceptible or resistant to breakdown and discuss how communities harbouring mutualisms may be affected by these evolutionary responses. We propose a template for evolutionary research on mutualism resilience and identify conservation approaches that may help conserve targeted mutualisms in the face of environmental change.

[1]  A. Traveset,et al.  Conservation and restoration of plant–animal mutualisms on oceanic islands , 2010 .

[2]  Jordi Bascompte,et al.  Plant-Animal Mutualistic Networks: The Architecture of Biodiversity , 2007 .

[3]  L. Harder,et al.  Floral adaptation and diversification under pollen limitation , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[4]  Richard Karban,et al.  Breakdown of an Ant-Plant Mutualism Follows the Loss of Large Herbivores from an African Savanna , 2008, Science.

[5]  Michelle E. Afkhami,et al.  Symbiosis Lost: Imperfect Vertical Transmission of Fungal Endophytes in Grasses , 2008, The American Naturalist.

[6]  E. Allen,et al.  MYCORRHIZAL COMMUNITY DYNAMICS FOLLOWING NITROGEN FERTILIZATION: A CROSS‐SITE TEST IN FIVE GRASSLANDS , 2007 .

[7]  J. Thompson The Geographic Mosaic of Coevolution , 2005 .

[8]  R. Frankham,et al.  Estimating the Potential for Adaptation of Corals to Climate Warming , 2010, PloS one.

[9]  Juan M Morales,et al.  Invasive Mutualists Erode Native Pollination Webs , 2008, PLoS biology.

[10]  Ørjan Totland,et al.  How does climate warming affect plant-pollinator interactions? , 2009, Ecology letters.

[11]  J. Bascompte,et al.  Global change and species interactions in terrestrial ecosystems. , 2008, Ecology letters.

[12]  P. Jordano,et al.  Differential contribution of frugivores to complex seed dispersal patterns , 2007, Proceedings of the National Academy of Sciences.

[13]  J. Biesmeijer,et al.  Global pollinator declines: trends, impacts and drivers. , 2010, Trends in ecology & evolution.

[14]  D. Doak,et al.  Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism , 2010, Proceedings of the National Academy of Sciences.

[15]  C. Mahaffey The conundrum of marine N2 fixation , 2005 .

[16]  Jordi Bascompte,et al.  Non-random coextinctions in phylogenetically structured mutualistic networks , 2007, Nature.

[17]  A. Griffin,et al.  Evolutionary Explanations for Cooperation , 2007, Current Biology.

[18]  Emmanuelle Porcher,et al.  Plant mating systems in a changing world. , 2010, Trends in ecology & evolution.

[19]  H. Vasconcelos,et al.  Long-term persistence of a neotropical ant-plant population in the absence of obligate plant-ants. , 2009, Ecology.

[20]  E. Siemann,et al.  The effects of soil biota and fertilization on the success of Sapium sebiferum , 2008 .

[21]  M. Aizen,et al.  A meta-analysis of bees' responses to anthropogenic disturbance. , 2009, Ecology.

[22]  C. Gómez,et al.  Consequences of the Argentine ant, Linepithema humile (Mayr), invasion on pollination of Euphorbia characias (L.) (Euphorbiaceae) , 2005 .

[23]  B. Wang,et al.  Phylogenetic distribution and evolution of mycorrhizas in land plants , 2006, Mycorrhiza.

[24]  Bob W. Kooi,et al.  Adapt or disperse: understanding species persistence in a changing world , 2010 .

[25]  E. Kiers,et al.  Sanctions, Cooperation, and the Stability of Plant-Rhizosphere Mutualisms , 2008 .

[26]  MULTIPLE MUTUALISTS PROVIDE COMPLEMENTARY BENEFITS TO THEIR SEAWEED HOST , 2005 .

[27]  P. Abbot,et al.  Phytophagous Insect–Microbe Mutualisms and Adaptive Evolutionary Diversification , 2008, Evolution; international journal of organic evolution.

[28]  R. van Woesik,et al.  Phenotypic Variance Predicts Symbiont Population Densities in Corals: A Modeling Approach , 2010, PloS one.

[29]  H. Higuchi,et al.  Re-established mutualism in a seed-dispersal system consisting of native and introduced birds and plants on the Bonin Islands, Japan , 2009, Ecological Research.

[30]  P. Hallock Symbiont-bearing Foraminifera , 1999 .

[31]  S. Sim,et al.  Rapid evolution of flowering time by an annual plant in response to a climate fluctuation , 2007, Proceedings of the National Academy of Sciences.

[32]  C. A. Howell,et al.  Re-Shuffling of Species with Climate Disruption: A No-Analog Future for California Birds? , 2009, PloS one.

[33]  N. Moran,et al.  Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. , 2010, Annual review of entomology.

[34]  F. Kjellberg,et al.  Range Expansion Drives Dispersal Evolution In An Equatorial Three-Species Symbiosis , 2009, PloS one.

[35]  Michael E Hochberg,et al.  Coevolution of symbiotic mutualists and parasites in a community context. , 2007, Trends in ecology & evolution.

[36]  S. Carpenter,et al.  Global Consequences of Land Use , 2005, Science.

[37]  M. Grube,et al.  Joint Dispersal Does Not Imply Maintenance of Partnerships in Lichen Symbioses , 2009, Microbial Ecology.

[38]  Tibor,et al.  TREE RECRUITMENT IN AN EMPTY FOREST , 2011 .

[39]  Egbert J. de Vries,et al.  Diet–dependent effects of gut bacteria on their insect host: the symbiosis of Erwinia sp. and western flower thrips , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[40]  D. Aanen,et al.  High Symbiont Relatedness Stabilizes Mutualistic Cooperation in Fungus-Growing Termites , 2009, Science.

[41]  R. Steneck,et al.  Coral Reefs Under Rapid Climate Change and Ocean Acidification , 2007, Science.

[42]  M. McGeoch,et al.  Rapid range expansion and community reorganization in response to warming , 2008 .

[43]  David P Edwards The roles of tolerance in the evolution, maintenance and breakdown of mutualism , 2009, Naturwissenschaften.

[44]  Jane Memmott,et al.  The impact of an alien plant on a native plant-pollinator network: an experimental approach. , 2007, Ecology letters.

[45]  L. Cavieres,et al.  The presence of a showy invasive plant disrupts pollinator service and reproductive output in native alpine species only at high densities , 2008 .

[46]  D. Simberloff,et al.  Positive Interactions of Nonindigenous Species: Invasional Meltdown? , 1999, Biological Invasions.

[47]  E. Kiers,et al.  Selective flower abortion maintains moth cooperation in a newly discovered pollination mutualism. , 2010, Ecology letters.

[48]  Corey J A Bradshaw,et al.  Synergies among extinction drivers under global change. , 2008, Trends in ecology & evolution.

[49]  Louie H. Yang,et al.  Phenology, ontogeny and the effects of climate change on the timing of species interactions. , 2010, Ecology letters.

[50]  E. Simms,et al.  Pathways to mutualism breakdown. , 2006, Trends in ecology & evolution.

[51]  R. Gates,et al.  Functional diversity in coral–dinoflagellate symbiosis , 2008, Proceedings of the National Academy of Sciences.

[52]  Anthony R. Ives,et al.  Species Response to Environmental Change: Impacts of Food Web Interactions and Evolution , 2009, Science.

[53]  David J. Lohman,et al.  Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants , 2009, Proceedings of the National Academy of Sciences.

[54]  R. Bshary,et al.  Asymmetric cheating opportunities and partner control in a cleaner fish mutualism , 2002, Animal Behaviour.

[55]  K. Redford The Empty Forest Many large animals are already ecologically extinct in vast areas of neotropical forest where the vegetation still appears intact , 1992 .

[56]  M. Galetti,et al.  Big Fish are the Best: Seed Dispersal of Bactris glaucescens by the Pacu Fish (Piaractus mesopotamicus) in the Pantanal, Brazil , 2008 .

[57]  A. Ragazzi,et al.  Fungal endophytes in Mediterranean oak forests: a lesson from Discula quercina. , 2008, Phytopathology.

[58]  Todd C. LaJeunesse,et al.  Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral ‘bleaching’ event , 2009, Proceedings of the Royal Society B: Biological Sciences.

[59]  Alan E. Wilson,et al.  Mutualisms and aquatic community structure: The enemy of my enemy is my friend , 2004 .

[60]  R. Callaway,et al.  Soil biota and invasive plants. , 2006, The New phytologist.

[61]  L. Lach Argentine ants displace floral arthropods in a biodiversity hotspot , 2007 .

[62]  P. Jordano,et al.  Seed Dispersal Anachronisms: Rethinking the Fruits Extinct Megafauna Ate , 2008, PloS one.

[63]  D. Goulson Effects of introduced bees on native ecosystems , 2003 .

[64]  Anna Traveset,et al.  Biological invasions as disruptors of plant reproductive mutualisms. , 2006, Trends in ecology & evolution.

[65]  Jordi Bascompte,et al.  The assembly and disassembly of ecological networks , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[66]  Denis Couvet,et al.  Evolutionary Conservation Biology , 2009 .

[67]  Seán G. Brady,et al.  Recent and simultaneous origins of eusociality in halictid bees , 2006, Proceedings of the Royal Society B: Biological Sciences.

[68]  R. Callaway,et al.  Mycorrhizae transfer carbon from a native grass to an invasive weed: evidence from stable isotopes and physiology , 2004, Plant Ecology.

[69]  Hideyuki Doi,et al.  Heterogeneous intra-annual climatic changes drive different phenological responses at two trophic levels , 2008 .

[70]  A. Valiente‐Banuet,et al.  Modern Quaternary plant lineages promote diversity through facilitation of ancient Tertiary lineages , 2006, Proceedings of the National Academy of Sciences.

[71]  E. Mondor,et al.  Do exaptations facilitate mutualistic associations between invasive and native species? , 2007, Biological Invasions.

[72]  B. Soden,et al.  Atmospheric Warming and the Amplification of Precipitation Extremes , 2008, Science.

[73]  U. Mueller,et al.  The Evolution of Agriculture in Insects , 2005 .

[74]  R. Bustamante,et al.  Does human-induced habitat transformation modify pollinator-mediated selection? A case study in Viola portalesia (Violaceae) , 2010, Oecologia.

[75]  S. Jackson,et al.  Novel climates, no‐analog communities, and ecological surprises , 2007 .

[76]  I. Sanders,et al.  Changes in arbuscular mycorrhizal fungal phenotypes and genotypes in response to plant species identity and phosphorus concentration. , 2009, The New phytologist.

[77]  M. Rillig,et al.  Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. , 2009, Ecology letters.

[78]  D. O'dowd,et al.  New mutualism for old: indirect disruption and direct facilitation of seed dispersal following Argentine ant invasion , 2008, Oecologia.

[79]  J. Sperry,et al.  Tansley Review , 2022 .

[80]  R. Berkelmans,et al.  A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization , 2008, Proceedings of the Royal Society B: Biological Sciences.

[81]  Lian Pin Koh,et al.  The sixth mass coextinction: are most endangered species parasites and mutualists? , 2009, Proceedings of the Royal Society B: Biological Sciences.

[82]  T. Palmer SPATIAL HABITAT HETEROGENEITY INFLUENCES COMPETITION AND COEXISTENCE IN AN AFRICAN ACACIA ANT GUILD , 2003 .

[83]  H. Howe,et al.  Recruitment of Hornbill‐Dispersed Trees in Hunted and Logged Forests of the Indian Eastern Himalaya , 2009, Conservation biology : the journal of the Society for Conservation Biology.