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 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 Biodiversity, 2013

Chengjiang Small Shelly Fauna Fauna

Nama

White Sea – 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 Analysis

• Concatenated sequences: 7 different housekeeping genes (2055 aa) (Peterson et al. 2004) • 118 taxa representing all major metazoan • 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 ~ 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 Gene pool Gene pool Species 1

Genetic inheritance Ecosystem Engineering Natural selection Natural selection Spillover Ecological Spillover Ecological

E Ecological inheritance E t+1! t! Natural selection Natural selection

Species 2 Gene pool Gene pool

Genetic inheritance 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 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