Evolutionary Ecology of Weeds Evolutionary Ecology of Weeds Jack Dekker Weed Biology Laboratory Agronomy Department Iowa State University Ames, Iowa 50010 USA EMail: [email protected] WWW URL: www.public.iastate.edu/~jdekker 2011 ClassUse Version Copyright 1.1.11 Jack Dekker 1 Evolutionary Ecology of Weeds 2011 SHORT TABLE OF CONTENTS UNIT 1: THE NATURE OF WEEDS 13 1 The nature of weeds 14 1.1 What is a weed? 1.2 The definition of a weed 1.3 Weeds and human nature 1.4 Weedy traits 1.5 The origins of weeds 1.6 World origins and centers of agriculture, crop domestication and cultivation 1.7 World crop-weed species groups UNIT 2: THE EVOLUTION OF WEED POPULATIONS 45 2 Evolution, natural selection and weedy adaptation 47 2.1 Introduction 2.2 Evolution 2.3 Natural selection and elimination 2.4 The process of natural selection 2.5 Adaptation 3 Formation of the local weed population (deme): Precondition to natural selection 55 3.1 Introduction: opportunity and the formation of the local deme 3.2 The structure of local weedy opportunity 3.3 Habitat heterogeneity and dynamics 3.4 Limiting resources and pervasive conditions in local opportunity 3.5 The nature of plant invasions of local opportunity 4 Generation of genotypic and phenotypic variation: First process of natural selection 79 4.1 Genotypes and phenotypes 4.2 Generate genetic variation 4.3 Generate phenotypic variation 5 Survival, reproduction and inheritance: Second process of natural selection 97 5.1 Survive, Avoid Mortality 5.2 Reproduce the fittest, eliminate the others 5.3 Inheritance: transmit parental traits to offspring UNIT 3: ADAPTATION IN WEED LIFE HISTORY 114 6 Weed life history 115 6.1 Introduction to life history 6.2 Plant life history classification systems 6.3 Representing weed life history 6.4 The ecological demography of plant population life history dynamics 6.5 Evolutionary, trait-based, weed life history population dynamics 7 Reproductive adaptation 137 7.1 Introduction 7.2 Flowering, anthesis, fertilization and birth 7.3 Embryo adaptation: embryogenesis and dormancy induction 7.4 Propagule adaptation: post-abscission fecundity 8 Propagule dispersal in space and time 157 8.1 Introduction 8.2 Dispersal in space 8.3 Dispersal in time: formation of seed pools in the soil 8.4 Propagule germination and recruitment 2 Evolutionary Ecology of Weeds UNIT 4: ADAPTATION IN LOCAL PLANT COMMUNITIES 182 Weed-crop communities as complex adaptive systems 9 Neighbor interactions in local plant communities 186 9.1 Adaptation to neighbors in the community 9.2 The nature of neighbor interactions in the community 9.3 Strategic roles and traits of interference and facilitation with neighbors 9.4 Effects of neighborhood interactions on plant density, growth and form 10 Weed community structure, dynamics and biodiversity 209 10.1 Weed communities 10.2 Weed community structure 10.3 Exploiting opportunity: weed community dynamics 10.4 Weed community biodiversity 3 Evolutionary Ecology of Weeds 2011 TABLE OF CONTENTS & SYLLABUS Forward 9 Introduction 11 UNIT 1: THE NATURE OF WEEDS 13 1 The nature of weeds 14 Summary 1.1 What is a weed? 1.2 The definition of a weed 1.3 Weeds and human nature 1.4 Weedy traits 1.5 The origins of weeds 1.5.1 Weeds, planting and crop domestication 1.5.2 Biogeographic prehistory of agriculture 1.5.3 Pre-agricultural preadapted wild colonizing species 1.5.4 Wild-crop-weed complexes 1.6 World origins and centers of agriculture, crop domestication and cultivation 1.7 World crop-weed species groups UNIT 2: THE EVOLUTION OF WEED POPULATIONS 45 Introduction 2 Evolution, natural selection and weedy adaptation 47 Summary 2.1 Introduction 2.2 Evolution 2.2.1 Micro- and macroevolution 2.2.2 Units of evolution and natural selection 2.3 Natural selection and elimination 2.4 The process of natural selection 2.4.1 Population formation: Precondition to natural selection 2.4.2 Generate variation: Process of natural selection, step 1 2.4.3 Survival and reproduction: Process of natural selection, step 2 2.5 Adaptation 3 Formation of the local weed population (deme): Precondition to natural selection 55 Summary 3.1 Introduction: opportunity and the formation of the local deme 3.2 The structure of local weedy opportunity 3.2.1 Weedy habitats 3.2.2 Niches in the local community 3.2.3 The niche hypervolume 3.3 Habitat heterogeneity and dynamics 3.3.1 Spatial heterogeneity and patchiness 3.3.2 Temporal division of the environment 3.3.3 Disturbance 3.4 Limiting resources and pervasive conditions in local opportunity 3.4.1 Limiting resources 3.4.1.1 Light 3.4.1.2 Water 3.4.1.3 Mineral nutrients 3.4.1.4 Gases 3.4.2 Pervasive conditions in the environment 3.4.2.1 Heat 3.4.2.2 Terroir 3.4.3 Environmental signal spacetime 4 Evolutionary Ecology of Weeds 3.5 The nature of plant invasions of local opportunity 3.5.1 The plant invasion process: seizing, exploiting and occupying opportunity 3.5.2 Dispersal 3.5.3 Colonization 3.5.4 Enduring occupation of a locality 3.5.5 Extinction 3.5.6 The perception of plant invasion 4 Generation of genotypic and phenotypic variation: First process of natural selection 79 Summary 4.1 Genotypes and phenotypes 4.2 Generate genetic variation 4.2.1 Sources of genetic diversity 4.2.1.1 Forces increasing population variability 4.2.1.2 Forces decreasing population variability 4.2.2 Speciation 4.2.2.1 Process of speciation 4.2.2.2 Reproductive isolating mechanisms 4.2.2.3 Modes of speciation 4.3 Generate phenotypic variation 4.3.1 Phenotypic plasticity 4.3.2 Somatic polymorphism 5 Survival, reproduction and inheritance: Second process of natural selection 97 Summary 5.1 Survive, Avoid Mortality 5.2 Reproduce the fittest, eliminate the others 5.2.1 Timing of reproduction 5.2.2 Plant age and stage structure 5.2.3 Reproductive value 5.2.4 Risk of death determines life history 5.2.5 Influences of plant density on mortality 5.2.6 Modes of selection and population diversity 5.3 Inheritance: transmit parental traits to offspring 5.4 Mating system and inheritance 5.4.1 Mating system and opportunity 5.4.2 Evolution of mating systems 5.4.3 Sex classification systems 5.4.4 Types of mating systems 5.4.4.1 Self-pollenating species 5.4.4.2 Out-crossing species 5.4.4.3 Apomictic species 5.4.4.4 Vegetative clone reproducing species UNIT 3: ADAPTATION IN WEED LIFE HISTORY 114 Introduction 6 Weed life history 115 Summary 6.1 Introduction to life history 6.1.1 Phenotypic life history traits 6.1.2 Processes of life history adaptation 6.2 Plant life history classification systems 6.2.1 Life span 6.2.2 Growth and life form 6.2.3 Life history strategies 6.3 Representing weed life history 6.4 The ecological demography of plant population life history dynamics 6.4.1 Weed life history models 6.4.2 Demographic weed life history population dynamics models 6.4.3 Representation and information, inference and prediction 5 Evolutionary Ecology of Weeds 6.4.3.1 Representation and information 6.4.3.2 Inference 6.4.3.2.1 The deme 6.4.3.2.2 Life history development and behavior 6.4.3.2.3 Model formalization and measurement metrics 6.4.3.3 Predicting weed population dynamics 6.5 Evolutionary, trait-based, weed life history population dynamics 7 Reproductive adaptation 137 Summary 7.1 Introduction 7.2 Flowering, anthesis, fertilization and birth 7.2.1 Parental plant architecture 7.2.2 Mating systems 7.3 Embryo adaptation: embryogenesis and dormancy induction 7.3.1 Induction of seed dormancy 7.3.2 The evolutionary ecology of seed dormancy 7.3.3 Weed seed dormancy variability and somatic polymorphism 7.3.4 Evolutionary ecology of seed heteroblasty 7.3.5 Weed species seed heteroblasty examples 7.3.6 Observable seed dormancy-germinability regulation life forms 7.3.6.1 Non-dormant 7.3.6.2 Vegetative, perinating buds 7.3.6.3 Environmental seed germination control mechanisms 7.3.6.4 Hard, gas- and water-impermeable, seed envelope germination inhibition 7.3.6.5 Light-phytochrome and nitrate stimulated germination 7.3.6.6 Species with multiple interacting germination control mechanisms 7.3.6.7 Other seed germination control mechanisms 7.3.7 Experimental weed seed science 7.4 Propagule adaptation: post-abscission fecundity 150 7.4.1 Five roles of seeds 7.4.2 Principle of strategic allocation 7.4.3 Trade-offs among seed roles 7.4.4 Seed size trade-offs 7.4.4.1 Seed size plasticity and stability 7.4.4.2 Relationship of seed size to habitat 8 Propagule dispersal in space and time 157 Summary 8.1 Introduction 8.1.1 The evolutionary ecology of dispersal structures 8.1.2 Seed dispersal trade-offs 8.1.3 Cost of dispersal 8.1.4 Space-time dimensions of dispersal 8.2 Dispersal in space 8.2.1 Dispersal and post-dispersal processes 8.2.2 Seed flux at a locality 8.2.3 Modes of seed and propagule dispersal 8.2.3.1 Gravity 8.2.3.2 Wind and air 8.2.3.3 Water 8.2.3.4 Animal, non-human 8.2.3.5 Human 8.2.3.6 Other modes of dispersal 8.3 Dispersal in time: formation of seed pools in the soil 8.3.1 Adaptative roles of soil seed pools 8.3.2 Population dynamics in the soil seed pool 8.3.2.1 Life history of a seed 6 Evolutionary Ecology of Weeds 8.3.2.2 Seed states, fates and seed state transition processes 8.3.2.3 Seed pool additions, losses and continuity 8.3.3 Structure of soil seed pools 8.3.3.1 Spatial distribution in the soil profile 8.3.3.2 Floral seed community compostion 8.3.3.3 Seed pool size 8.3.3.4 Seed longevity in the soil 8.4 Propagule germination and recruitment 8.4.1 Introduction 8.4.2 Process of recruitment 8.4.3 Germination micro-sites and safe sites 8.4.4 Patterns of seedling emergence 8.4.5 Relationship between seed heteroblasty and recruitment timing UNIT 4: ADAPTATION IN LOCAL PLANT COMMUNITIES 182 Introduction Weed-crop communities as complex adaptive systems 9 Neighbor interactions in local plant communities 186 Summary 9.1 Adaptation to neighbors in the community 9.2 The nature of neighbor interactions in the community 9.2.1 Patterns of neighbor interactions 9.2.2 Interference interactions between neighbors 9.2.2.1 Competition 9.2.2.2 Amensalism 9.2.2.3 Antagonism 9.2.3 Facilitative interactions between neighbors 9.2.3.1 Mutualism 9.2.3.2 Commensalism 9.3 Strategic roles and traits of interference and facilitation with neighbors 9.3.1 Strategic roles and traits of interference with neighbors 9.3.1.1 Spatial foraging for local opportunity 9.3.1.2 Temporal foraging for local opportunity 9.3.2 Strategic roles and traits of facilitation with neighbors 9.3.2.1 Escape and avoid neighbors 9.3.2.2 Co-exist with neighbors 9.3.2.3 Co-operate with neighbors 9.4 Effects of neighborhood interactions on plant density, growth and form 9.4.1 Space, neighborhoods and plant density 9.4.2 Plant density and productivity per unit area. 9.4.3 Plant density and plant size 9.4.4 Plant density and plant form 9.4.5 Dangers in plant density demography 10 Weed community structure, dynamics and biodiversity 209 Summary 10.1 Weed communities 10.2 Weed community structure 10.2.1 The origins of weeds: wild-crop-weed plant complexes 10.2.2 Biogeographical population genetic structure 10.2.3 Genotype structuring: species association for weedy colonization 10.2.3.1 Species-groups 10.2.3.2 Polyploid species clusters 10.2.3.3 Aggregate species 10.2.4 Genotype structuring: pre-adaptive coloninzing achetypes 10.2.4.1 Generalist-specialist genotypes 10.2.4.2 Genetic-reproductive colonizing types 10.3 Exploiting opportunity: weed community dynamics 10.3.1 Ecological roles-guilds-trades in weed-crop plant communities 10.3.1.1 Guild structure and community organization 7 Evolutionary Ecology of Weeds 10.3.1.2 Parameters of weed species ecological role and niche 10.3.1.3 Trait guild: relative seedling/bud emergence order 10.3.2 Changes in plant community structure 10.3.2.1 Weed population shifts 10.3.2.2 Plant community ecological succession 10.4 Weed community biodiversity 10.4.1 Scales of weedy biodiversity 10.4.2 Biodiversity encountered by interacting neighbors 10.4.3 Weed community biodiversity: complexity, stability and equilibrium 10.4.3.1 Community complexity 10.4.3.2 Community stability 10.4.3.3 Equilibrium in the community 10.4.4 Conclusions APPENDICES 236 I. Biology of weeds 237 II. Weed casebook studies 238 Appendix 1: Weedy Setaria species-group 1A: The population genetic structure of the weedy Setaria species-group 239 1B: FoxPatch: An evolutionary model system for weedy Setaria species-group seed life history dynamics 242 1C: Relationship of Setaria seed heteroblasty and seedling recruitment 252 III. Essays 257 Appendix 2: The perception of plant invasion (from Chapter 3) 257 GLOSSARY 262 SELECTED READINGS 288 REFERENCES CITED 289 INDEX 302 8 Evolutionary Ecology of Weeds FORWARD: 2011 Weeds are plants too. The principles of weedy invasion and colonization are same as for all plants regardless of the time they appear in a locality during ecological succession. Weeds colonize disturbed unoccupied opportunity spacetime, while later successional species colonize opportunity spacetime created by earlier-appearing species in those same localities. The same underlying processes and locality pertain, only the traits and opportunity change. On the shoulders of giants. Harper‘s ‗Population Biology of Plants‘ (1977) provided a broad view of plant biology, especially weed biology. It is now out of print. This textbook was the original source I used in developing and teaching Agronomy 517, Weed Biology, since 1992. There is no replacement that provides the scope and detail this classic reference provided. In the intervening years I borrowed much of Harper‘s concepts in this book. I also relied on Jonathan Silvertown‘s two demographic-centric textbooks (Silvertown and Doust, 1993; Silvertown and Charlesworth, 2001) to fill out the scope of that course. Learning from students. The contributions of all past graduate students in Agronomy 517 (and now 417 for undergraduates), from 1992 to present, have been a crucial component in the development of this book. Student projects, often focused on a single weed species, as well as student discussions, questions, insights (especially those from their own experience) and examination responses have strongly influenced the evolution of this course and this book. By definition. Scientific jargon is informative, extensive and can be very confusing. Scientific terminology often has different meanings in different disciplines. Terms are sometimes used promiscuously, causing misunderstanding and often leading to incorrect mental models of how systems work (e.g. invasive species (Appendix 2) and biodiversity). For this reason, definitions of most of the important concepts are provided, with alternative meanings provided to highlight where confusion and misunderstanding within the sciences arises (e.g. trait, Violee et al., 2007). Discussion of these differing usages can provide much insight in the classroom. Understanding the variety of student perspectives on definitions is gained by this comparative etymology. Out of Iowa. The background and experience of the author is centered on the mid- continent North American agricultural areas, including those of the United States ‗Corn Belt‘ and grain producing areas of eastern and western Canada. Extensive Eurasian travel, germplasm collection, research and teaching in areas outside of the U.S. and Canada have enriched this perspective. My research experience with the weedy foxtails, Setaria species-group, provides a model system to explain weedy concepts throughout book (Appendix 1). Weed Science as a discipline encourages species community understandings, with far less emphasis on the biology of individual species (or closely related species groups), a disciplinary mode more common in Entomology and Plant Pathology. Communities are the emergent behaviors arising from individuals in these complex adaptative systems. Both perspectives provide insights into the workings of weed communities. 9 Evolutionary Ecology of Weeds Model representation. Ecology often utilizes demographic models, while evolutionary models of weed behavior emphasize the central role adaptive functional traits play in community behavior and change. Both perspectives must be understood in depth, and seen as an integrated whole, to fully understand agricultural weed communities. The conceptual limitations and intellectual liberations of both types of models are also a focus in this book. New for 2011. This new version of the book (2011) continues to be guided by evolutionary principles clearly elucidated by Ernst Mayr in ―What Evolution Is‖ (2001), especially his clear presentation of the component processes and conditions by which natural selection operates in biological systems. It is this that has provided the structural organization of this book. This new version contains a new chapter 1 attempting to define more clearly the nature of weeds. As such the anthropological role of humans and the origins of agriculture are featured. The consequences of agriculture are the important world crop- weed groups (table 1.4) that now plague us. This first unit of this book shows the origins of these groups. Chapter 10 comes full circle from table 1.4 and explores local weed-crop communities in more detail, as complex adaptative systems. Between these two units/chapters, units 2, 3 and chapter 9 elucidate the evolution of weeds and their consequential life history attributes. Book?, or just very detailed class notes? This version is an incomplete book, a work in progress, a glass half-full. 10