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Evolution of Ecological Communities Through the Lens of an Island Chronosequence

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Evolution of Ecological Communities Through the Lens of an Island Chronosequence Evolution of ecological communities through the lens of an island chronosequence Rosemary Gillespie, Henrik Krehenwinkel, Andy Rominger Jun Ying Lim, Kari Goodman, Dan Gruner, John Harte University of California, Berkeley, USA NSF Dimensions of Biodiversity nature.berkeley.edu/evolab nature.berkeley.edu/hawaiidimensions Evolution of ecological communities through the lens of an island chronosequence Andy Rominger, Henrik Krehenwinkel, Dan Gruner, Jun Ying Lim, Kari Goodman, Ellie Armstrong, Gordon Bennett, Michael Henrik Brewer, Darko Cotoras, Curtis Ewing, Diana Percy, Patrick Krehenwinkel O’Grady, Don Price, George Roderick, Kerry Shaw Biodiversity Dynamics Fitness Fitness Microevolution Macroevolution Fitness Evolution Ecology Fitness Biodiversity dynamics Processes occur over different scales, so how to assess dynamics? Island chronosequence 5.1 my 2.6-3.7 my 0.7-1.8 my 0-0.4 my Dynamics of trait evolution Species diversity through time blue- extant lineages only Extant & extinct lineages (brown line) brown - extant & extinct lineages. extant lineages (blue line) Circles - true & reconstructed trait value Temporal dynamics in niche interactions for the most recent common ancestor Geographic space Environmental space Neontological & paleontological data Time Species shifts from orange to blue environment that appears only after T1 Environmental factor 1 Fritz et al 2013. Diversity in time and space... TREE 28, 509-516 Chronosequence 5 million years ago Necker Nihoa Kauai Niihau 2.5 million years ago Nihoa Kauai Oahu Niihau 1 million years ago Niihau Kauai Oahu Maui Nui Necker 5 million years ago Nihoa Kauai Niihau 2.5 million years ago Nihoa Kauai Oahu Niihau 1 million years ago Niihau Kauai Oahu Maui Nui 0.5 million years ago Kauai Niihau Oahu Maui Nui Can read chrono-sequence as a fossil record to look Hawaii at: Present Kauai • Dynamics of trait evolution Niihau • Species diversity through Maui Nui Oahu time • Temporal dynamics in niche interactions. Hawaii Island chronosequence 1. Microevolution 2 macroevolution 1. Evolutionary dynamics over time • Repetition of evolutionary process 2. Species diversity through time • How communities come together over time 3. Ecological interactions • Measurement of ecological metrics (space for time) 1. Micro- to macro-evolution • the early stages 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Youngest island ….. Dynamics on Hawaii Island as the “crucible of evolution” Carson et al. 1990 PNAS 87, pp. 7055-7057, 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Habitat fragmentation clearly limits gene flow Photograph by J.D. Griggs Forest habitat specialist Vandergast et al. 2004. Mol Ecol 13: 1729-1743 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Balance between isolation & time Isolation separates populations Fusion injects diversity How does this play out over time? 2. Evolutionary dynamics blue- extant lineages only brown - extant & extinct lineages. 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Evolutionary Dynamics 5.1 my 2.6-3.7 my 0.7-1.8 my Progression rule 0-0.4 my 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Hormiga, Arnedo & Gillespie 2003. Systematic Biology 52: 70-88 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions M. anguliventris Hawaii Diversification M. anguliventris Maui M. anguliventris Oahu early in radiation M. anguliventris Kauai • Adaptive M. naevigera Hawaii • Populations diverge M. naevigera Maui in allopatry M. naevigera Oahu M. discreta Molokai M. discreta Kauai M. cavata Hawaii M. cavata Necker M. nigrofrenata Hawaii M. nigrofrenata Kauai M. rufithorax Oahu M. imbricataOahu M. facunda Hawaii M. arida Maui M. sp Maui M. kanakana Hawaii M. kanakana Maui M. kanakana Oahu M. kanakana Kauai M. spinosa Oahu M. hiatus Maui M. perkinsi Oahu Garb & Gillespie, 2009. M. edita Oahu Molecular Ecology Radiation of long-jawed spiders, Tetragnatha, in Hawaii 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Based on mtDNA, minisatellites, & allozymes ….. ….. general progression down island chain Independent evolution of ecomorphs Hawaii Maui Nui Oahu Kauai Gillespie 2004, Science; Pons & Gillespie 2004. J. Mol Evolution 59: 632-641 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Argyrodes trigonum A. huinakolu Kauai Evolution of A. kahili Kauai “ecomorphs” A. uwepa Oahu A. sp (white) Oahu A. makue Oahu Repeated evolution A. sp (black) Molokai A. sp (gold) Molokai A. sp Molokai (like mele- kalikimaka) A. poele Molokai Gold – under leaves Gene-tree (mt A. melekalikimaka Maui COI & A. laau Maui nuclear EF1 A. alepe Maui White – seqs); output A. corniger Maui on lichen by Beast. Posterior A. waikula Hawaii Brown – bark/ rock probabilities A. hiwa Hawaii above nodes Rhomphaea metaltissima Ariamnes attenuata Spintharus flavidus 2. Evolutionary dynamics blue- extant lineages only Ariamnes spiders brown - extant & extinct lineages. “Onset” of diversification in a given lineage is reset on each island 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Therefore, we know that: • Taxa differ in • The interplay between ecological & genetic shifts during diversification • …. Can now look at patterns of diversity over time; whole communities 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions 3. Species Diversity Extant & extinct lineages (brown line) extant lineages (blue line) 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Insights from chronosequence Orsonwelles Mecaphesa 4 8 3.5 7 3 6 2.5 5 2 4 1.5 3 1 2 0.5 1 No. species/area 0 0 Hawaii Maui Nui Oahu Kauai Hawaii Maui Nui Oahu Kauai Youngest -- Island age -- Oldest Youngest -- Island age -- Oldest 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Insights from chronosequence Orsonwelles Mecaphesa 4 8 3.5 7 3 6 2.5 5 2 4 1.5 3 1 2 0.5 1 No. species/area 0 0 Hawaii Maui Nui Oahu Kauai Hawaii Maui Nui Oahu Kauai Ariamnes Tetragnatha – spiny leg clade 4.5 3 4 2.5 3.5 3 2 2.5 1.5 2 1.5 1 1 0.5 0.5 No. species/ area No. species/ 0 0 Hawaii Maui Nui Oahu Kauai Hawaii Maui Nui Oahu Kauai Youngest -- Island age -- Oldest Youngest -- Island age -- Oldest 0.025 Insights from chronosequence 0.02 R2 = 0.996 R2 = 0.8088 R2 = 0.9951 a 0.015 e r a / s e i c e p s . R2 = 0.8403 o N 0.01 R2 = 0.9917 No. Species/Area R2 = 0.9575 0.005 R2 = 0.9641 R2 = 0.96 R2 = 0.8238 0 0 1 2 3 4 5 6 Gillespie & Baldwin 2009 IslandIsland Age Age (My) Species diversity over time Chronosequence Extant & extinct lineages (brown line) extant lineages (blue line) 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Therefore, we know that: • Taxa differ in • The interplay between ecological & genetic shifts during diversification • Rate of accumulation of species • Patterns of diversity over time • Highlights how different groups perceive the chronosequence • …. and ecological theory can give us a guide as to what’s novel 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions 4. Ecological Interactions • Measurement of ecological metrics • Space for time Geographic space Environmental space Different environmental conditions (colors) Species (*) shifts from Time orange to blue environment that appears only after T1 Environmental factor 1 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Maximum Entropy Theory of Ecology • Community-wide genetic divergence across space, environment and time (chronosequence) • Testing novel theory Species Individuals Energy Harte (2011) Oxford University Press. 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Fitting species abundance data to METE predictions Deviation from predictions on youngest substrates may indicate that community has not yet reached steady state Rominger et al. 2015 Global Ecology and Biogeography 1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Interaction Networks • Nestedness decreases with site age. Perhaps due to high immigration of new species with high probabilities to eat / be eaten by generalist species already present • Modularity increases, likely due to coevolution Modularity - degree to which species interact in semi- autonomous modules Nestedness - degree of asymmetry in interaction between specialists and generalists Rominger et al. 2015 Global Ecology and Biogeography Networks deviateKilauea most from KohalaMETE predictionsMaui on youngest &Kauai oldest sites 0 e 1 e r g e D ecol Incomplete specialization assembly 1 Linkage 1 . e 0 ● Cosmopolitans e r ● g Endemics e d ● ● ● d e z i l a m r o N More ….specialization … LessMore ….specialization… Linkage 0.001 0.010 0.100 1.000Bennett & O’Grady Age (mya) 2012 Mol. Phylo. Evol. • ecological theory can give us a guide as to what’s novel Top panels show that networks deviate most from MaxEnt on youngest and oldest sites. Deviation on Koh is not difRomingerfer entet al. 2015
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