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 Dubautia sandwicense reticulata ssp. macrocephalum 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 Chengjiang Small Shelly Fauna Fauna Nama White Sea – Ediacaran Avalon Doushantuo Embryos 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 Rapid early increase in disparity – Proterozoic/Cambrian acritarchs – Paleozoic gastropods – Paleozoic rostroconchs – Ordovician bryozoans – Crinoids – Paleozoic blastozoans – Ordovician trilobites – Marine arthropods diversityDiversity – Insects Disparity – Angiosperm pollen disparity 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 Monosiga Amphimedon Trichoplax Nematostella Drosophila genome 41.6 167 98 450 180 size (Mb) # 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. 5 6? 9 10 10 families 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 2" Species 1" Natural selection Natural selection Gene pool" t! Gene pool" Ecological" E Spillover" " " " Genetic inheritance Ecological inheritance Genetic inheritance Natural selection Natural selection t+1! Gene pool" Gene pool" Ecological" E Spillover 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 .