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. No. area species/
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. No. area species/
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 No.
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 the patter endemics on Hal nooverall. long show When a dif lookingincr at links to plantcosmopolitans. genera this patterEndemicsBottom show panel lowershowschance. linkage number Koh overall, of shows links butand forminimal significantly oldest island sites. modularityendemics DeviationT versus on island Koh is not dif op panels show that networks deviate most fr ease on the middle aged site Hal. Koh shows incr •
More ….specialization … Less sites & oldest on youngest METE predictions from most deviate Networks
ecological theory can give guide us a as to what’s novel Linkage n is driven in par Normalized degree Degree Linkage 0.1 1 10 assembly Incomplete ● Kilauea ● 0.001 Endemics Cosmopolitans t by plant diversity 0.010 Kohala fer Age (m Age ence in generality , and maximal connectance. y Rominger a) 0.100 fer . Maui ● ent than expected by et al. om MaxEnt on youngest 2015 Global Global Ecology and Biogeography eased linkage ● 1.000 specialization ecol n holds except that , indicating that 2012 2012 Mol. Bennett & O’Grady Kauai Phylo ● . Evol . Across the chronosequence we’ve found:
• Different arthropod groups perceive, colonize and diverge across evolving landscapes differently
• Results in different patterns of species accumulation over time
• Deviation from statistical steady state varies across groups and substrate ages.
• Interaction of ecological & evolutionary strategies, isolation & mixing, likely interact to produce patterns
1. Micro-macroevolution 2. Evolutionary dynamics 3.Species diversity 4. Ecological interactions Research Underway ……
Looking at sites of similar elevation, precipitation; all in Metrosideros forest and accessible in reserves
Biodiversity Dynamics Across a Chronosequence Intensive ecological sampling
Biodiversity Dynamics Across a Chronosequence Metagenomics across the chronosequence
Changes in Evolutionary Dynamics • Genetic structure of all lineages in the ecosystem • Which factors drive divergence of lineages
Changes in Community Structure & Dynamics • Rapid identification of taxa & cryptic diversity • Relative abundances • Using metabarcoding of whole predators to Henrik Krehenwinkel identify • prey-predator interactions • food plants of herbivores Zhou et al 2013. Ultra-deep sequencing enables high fidelity recovery of biodiversity for bulk arthropod samples without PCR amplification. GigaScience 2: 4. Pinol, J. et a. 2013. A progmatic approach to the analysis of diets of generalist predators …. Mol Ecol Resources 14: 18-26 Kozich et al. 2012 Applied & Environmental Microbiology Metagenomics across the chronosequence
• 16s based taxon identification • Molecular community studies • Also functional genomic studies • Initially on 454, now on MiSeq or HiSeq • ITS in fungi • COI in animals
Cost-effective mass-multiplexing • MiSeq protocol developed for microbiome sequencing • Applicable to any other PCR fragment; ~ 400 microbiome samples /run; sequencing right after PCR
Gibson, J. et al. 2014 Simultaneous assessment of the macrobiome & microbiome in a bulk sample of tropical arthropods. PNAS 111: 8007–8012 Ji, Y. Et al. 2013. Reliable, verifiable, and efficient … Ecology Letters 16:1245-1257 Yu, DW et al. Biodiversity soup ..2012. Methods in Ecology & Evolution 3: 613-623 Leray, M. & Knowlton, N. 2014. DNA barcoding & metabarcoding …. PNAS Mahalo! Thank you!
nature.berkeley.edu/hawaiidimensions
Visualization by Thorsten Andresen, Nils Sparwasser, S Reiniger & R Meisner; data from DLR, NGDC, GLCF & USGS