Innovation and Diversity Douglas H. Erwin National Museum of Natural History Smithsonian Institution Washington, DC USA
Questions What factors drive innovation, whether in biological, cultural or technological systems? Similar processes of variation, inheritance and selection and drift occur in all systems Understanding processes in one may shed light on the others Goal is to build models of innovation that span different systems
Hawaiian Silverswords
Adaptive Radiation of Hawaiian Silverswords Carlquistia California Argyroxiphium sandwicense ssp. macrocephalum Dubautia reticulata Dubautia waialealae Dubautia latifola All photos from Hawaiian Silversword Alliance website
THE CAMBRIAN EXPLOSION REPRESENTS THE CONSTRUCTION OF A DESIGN SPACE
THE CAMBRIAN EXPLOSION REPRESENTS THE CONSTRUCTION OF A DESIGN SPACE But how is this space constructed? Genes? Developmental Interactions? Ecological processes?
Erwin and Valentine, The Construction of Animal Biodiversity, 2013
Burgess Shale Small Shelly Fauna Chengjiang Fauna Nama Doushantuo Embryos Avalon White Sea Ediacaran Ediacaran Assemblages Trezona
Laflamme in prep.
Hurdia victoria Daley et al Science 2009
Anomalocaris
Aysheaia
Erwin and Valentine, The Cambrian Explosion, 2013
Erwin and Valentine, The Construction of Animal Biodiversity, 2013
Maximal Early Disparity Diversity diversity Disparity disparity Rapid early increase in disparity Proterozoic/Cambrian acritarchs Paleozoic gastropods Paleozoic rostroconchs Ordovician bryozoans Crinoids Paleozoic blastozoans Ordovician trilobites Marine arthropods Insects Angiosperm pollen time
IMPORTANCE OF GENOMIC AND DEVELOPMENTAL COMPLEXITY
Tree diagram of the birth, transfer, duplication and loss of key genes in the redox and electron transport pathways, in a founding burst of gene evolution between 3.3 and 2.7 billion years ago (David and Alm 2010).
Genomic Complexity genome size (Mb) Monosiga Amphimedon Trichoplax Nematostella Drosophila 41.6 167 98 450 180 # genes 9,100? 11,514 18,000 14,601 # cell types 1 12 4 20 50 # T.F. s? 57 35 min. 87 min. 87 # T.F. families 5 6? 9 10 10 microrna 0 8 0 40 152 (Erwin, 2009; Erwin & Valentine 2013)"
Erwin and Valentine, The Cambrian Explosion, 2013
Hypothetical Urbilaterian After Carroll et al 2001
Erwin and Valentine, The Cambrian Explosion, 2013
Molecular Clock Analysis Concatenated sequences: 7 different housekeeping genes (2055 aa) (Peterson et al. 2004) 118 taxa representing all major metazoan clades 24 calibration points: vertebrate + invertebrate Relaxed molecular clock analyses: CIR clock model in Phylobayes All estimates tested under various sensitivity analyses; all appear robust
Cryogenian" Ediacaran" Cambrian"
last common" ancestor (LCA) of all living animals" ~ 800 Ma" (732-840 Ma)"
LCA of cnidarians & bilaterians" ~ 700 Ma" (662-760 Ma)"
LCA of bilaterians" ~ 668 Ma" (641-773)"
last common" ancestor of all " living members" of the phylum"
Sea Urchin dgrn Biotapestry.org
Strongylocentrotus
Sea Urchin dgrn Biotapestry.org
Gene Regulatory Network Structure Erwin and Valentine, Forthcoming, 2012; after Davidson
Nature of Kernels Recursively wired regulatory genes Specify the spatial domain of a part of the developing embryo, often a regional pattern The kernels are dedicated to development and are not re-used elsewhere Interference with the function of any gene will destroy kernel function This forces subsequent evolutionary change either upstream or downstream of the kernel
Implications There is a structure to the network of developmental regulatory interactions Changes in some parts of regulatory networks are easier than in others Some types of changes, particularly the establishment of kernels, appears to have been easier early in metazoan evolution; these kernels are now highly refractory to modification
BUT GENES ALONE ARE NOT SUFFICIENT: THE ROLE OF ECOLOGY
Cambrian Predators Ottoia Anomalocaris Pikaia
Vertebrates ~ 515 Ma Nemerteans ~ 546 Ma Chaetognaths ~ 540 Ma
Fedonkin et al The Rise of Animals, 2007
Crassostrea virginica Image: WHOI
Ecosystem Engineering From Eric Heupel UConn.mp
Ecosystem Engineering Species 1" Gene pool" Natural selection Ecological" Spillover" Et! Natural selection Species 2" Gene pool" Genetic inheritance" Ecological inheritance" Genetic inheritance" Gene pool" Natural selection Ecological" Spillover Et+1! Natural selection Gene pool"
Types of Ecosystem Engineering Physical Engineering: Construction of physical structures (reefs, ) Chemical Engineering: Modification of the geochemical environment redox.
Cambrian Ecosystem Engineering Archaeocyathid reefs (+) Sponges & other filter feeders (+) Burrowed sediments (+/-) Shelly substrates (+) Mesoozooplankton (+)
IMPORTANCE OF MACROEVOLUTIONARY LAGS
Increase in mirna families; complexity of dgrn interactions Origin of Developmental Toolkit Origin of Eumetazoa Most signalling pathways present
Grassland Evolution
Grass Phylogeny Kellogg, 2001, Plant Physiology
Macroevolutionary Lags
Invention & Innovation Invention is the creation of something new and distinct (contrast with variation on established themes) Innovation occurs when inventions become economically or ecologically significant Joseph Schumpeter (1883-1950
FLICKERING OF INNOVATION IN EARLY HOMO SAPIENS If at first you don t succeed..
Chauvet Cave, France, 32,000 years old
How are new evolutionary spaces created? Potentiated by broader environmental setting (physical, genetic, ecologic) Actualized by genetic and developmental innovations leading to a new clade
Simpson t Adaptive Zones
How are new evolutionary spaces created? Potentiated by broader environmental setting (physical, genetic, ecologic) Actualized by genetic and developmental innovations leading to a new clade Refined by further developmental and ecological changes Realized as innovations by ecological expansion and evolutionary success