EVOLUTIONARY AND GENETIC BIOLOGY OF PRIMATES
CONTENTS DAVID G LLOYD AND THE EVOLUTION OF ?ORAL BIOLOGY: FROM NATURAL HISTORY TO STRATEGIC ANALYSIS 1 1 INTRODUCTION 1 2 BIOGRAPHICAL SKETCH 1 3 SELF- AND CROSS-FERTILIZATION IN PLANTS 1 3 1 EARLY INVESTIGATIONS ON MATING SYSTEMS 1 3 2 INTEGRATION OF POLLINATION AND MATING 1 4 GENDER STRATEGIES 1 4 1 EARLY INVESTIGATIONS OF PLANT SEXUAL DIVERSITY 1 4 2 THEORIES ON THE EVOLUTION OF SEXUAL SYSTEMS 1 4 3 GENDER CONCEPTS AND THEORY 1 5 ALLOCATION STRATEGIES 1 5 1 ALLOCATION TO COMPETING FUNCTIONS 1 5 2 SIZE-NUMBER COMPROMISES 1 5 3 APPLICATION TO SPECI?C PROBLEMS 1 6 FLORAL MECHANISMS 1 6 1 SEXUAL INTERFERENCE 1 6 2 THE EVOLUTION OF HETEROSTYLY 1 7 LLOYD’S EVOLUTION REFERENCES PART STRATEGIC PERSPECTIVES ON ?ORAL BIOLOGY SELECTION ON REPRODUCTIVE CHARACTERS: CONCEPTUAL FOUNDATIONS AND THEIR EXTENSION TO POLLINATOR INTERACTIONS 2 1 INTRODUCTION 2 2 PHENOTYPIC SELECTION ON REPRODUCTIVE STRATEGY 2 2 1 PHENOTYPIC SELECTION AND EVOLUTIONARY STABLE STRATEGIES 2 2 2 PHENOTYPIC SELECTION AND INHERITANCE OF QUANTITATIVE CHARACTERS 2 2 3 MEASURING PHENOTYPIC SELECTION 2 3 PLANT AND POLLINATOR INTERACTION 2 3 1 SPECIALIST OR GENERALIST? 2 3 2 POLLINATION AS TRADE 2 3 3 ECOLOGICAL DYNAMICS 2 4 SELF-FERTILIZATION, PHENOTYPIC SELECTION, AND REPRODUCTIVE ASSURANCE 2 4 1 ECOLOGICAL CONSEQUENCES OF SEL?NG MODE 2 4 2 EVOLUTIONARY CONSEQUENCES OF SEL?NG MODE 2 4 3 VARIABLE POLLINATION ENVIRONMENTS 2 5 DISCUSSION EVOLUTIONARILY STABLE REPRODUCTIVE INVESTMENT AND SEX ALLOCATION IN PLANTS 3 1 INTRODUCTION 3 2 THE CLASSIC MODEL OF SEX ALLOCATION FOR OUTCROSSING SPECIES 3 2 1 GAIN CURVES 3 2 2 ESS SEX ALLOCATION 3 2 3 EVOLUTION OF SEXUAL SYSTEMS 3 3 PLANT SIZE AND SEX ALLOCATION 3 3 1 BUDGET EFFECTS OF PLANT SIZE ON ?TNESS GAINS 3 3 2 DIRECT EFFECTS OF PLANT SIZE ON ?TNESS GAINS 3 3 3 WHY ARE MALE AND FEMALE FUNCTION OFTEN DISPLACED TEMPORALLY IN COSEXUAL PLANTS? 3 4 JOINT EVOLUTION OF REPRODUCTIVE EFFORT AND SEX ALLOCATION IN PERENNIAL PLANTS 3 4 1 SIZE-DEPENDENT REPRODUCTIVE EFFORT 3 5 DISCUSSION AND CONCLUSION POLLEN AND OVULE FATES AND REPRODUCTIVE PERFORMANCE BY ?OWERING PLANTS 4 1 INTRODUCTION 4 2 POLLEN FATES AND OVULE FATES 4 2 1 POLLEN DISPERSAL 4 2 2 POLLEN-TUBE GROWTH 4 2 3 OVULE FERTILIZATION 4 2 4 SEED DEVELOPMENT 4 2 5 SEEDLING ESTABLISHMENT AND PARENTAL ?TNESS 4 3 LIMITS ON SEED PRODUCTION 4 3 1 POLLEN LIMITATION 4 3 2 OVULE LIMITATION 4 3 3 RESOURCE LIMITATION 4 4 EXAMPLES OF THE ROLES OF POLLEN AND OVULE FATES IN ?ORAL AND MATING-SYSTEM EVOLUTION 4 4 1 IMPROVEMENTS IN POLLEN EXPORT 4 4 2 SIMULTANEOUS, AUTONOMOUS SELF-POLLINATION WITHOUT POLLEN DISCOUNTING 4 4 3 FACILITATED SELF-POLLINATION 4 4 4 DELAYED SELF-POLLINATION 4 5 CONCLUDING DISCUSSION 4 5 1 THE ASYMMETRY OF POLLEN AND OVULE FATES 4 5 2 LIMITS ON SEED PRODUCTION AND REPRODUCTIVE EVOLUTION ECOLOGICAL CONTEXT OF ?ORAL FUNCTION AND ITS EVOLUTION MODELS OF POLLINATOR-MEDIATED GENE DISPERSAL IN PLANTS 5 1 INTRODUCTION CONTENTS 5 2 THREE ICONIC PATTERNS OF POLLINATOR-MEDIATED GENE DISPERSAL 5 3 A HISTORICAL PERSPECTIVE ON THE THEORY OF POLLINATOR-MEDIATED GENE DISPERSAL 5 4 QUALITATIVE GENERALIZATIONS FROM THE PORTION-DILUTION MODEL 5 5 IN PURSUIT OF QUANTITATIVE PREDICTIONS FROM THE PORTION-DILUTION MODEL 5 6 EVOLUTIONARY BIOLOGY OF THE PATERNITY SHADOW 5 7 PROSPECTS FOR THE THEORY OF POLLINATOR-MEDIATED GENE DISPERSAL POLLINATOR RESPONSES TO PLANT COMMUNITIES AND IMPLICATIONS FOR REPRODUCTIVE CHARACTER EVOLUTION 6 1 INTRODUCTION 6 2 PROPERTIES OF PLANTS AND COMMUNITIES 6 3 PLANT-COMMUNITY EFFECTS ON POLLINATOR RESPONSES 6 3 1 POLLINATOR BEHAVIOURAL RESPONSES 6 3 2 POLLINATOR DEMOGRAPHIC RESPONSES 6 3 3 POLLINATOR-COMMUNITY STRUCTURE 6 4 CONSEQUENCES OF POLLINATOR RESPONSES FOR SELECTION ON PLANT REPRODUCTIVE TRAITS 6 4 1 HETEROSPECI?C POLLEN TRANSFER 6 4 2 POLLINATOR VISITATION RATE 6 4 3 POLLINATOR-COMMUNITY COMPOSITION 6 5 COMMUNITY CONTEXT AND MATING-SYSTEM EVOLUTION IN CLARKIA 6 5 1 STUDY SYSTEM 6 5 2 POLLINATOR RESPONSES TO CLARKIA COMMUNITIES 6 5 3 CONSEQUENCES OF COMMUNITY CONTEXT FOR SELECTION ON THE MATING SYSTEM 6 5 4 BIOGEOGRAPHIC PATTERNS OF MATING-SYSTEM VARIATION AND PLANT-COMMUNITY DIVERSITY 6 6 CONCLUSIONS AND FUTURE DIRECTIONS NON-POLLINATOR AGENTS OF SELECTION ON ?ORAL TRAITS 7 1 INTRODUCTION 7 2 SELECTION ON REPRODUCTIVE TRAITS BY NON-POLLINATOR AGENTS 7 2 1 PETAL COLOUR 7 2 2 FLOWER SHAPE 7 2 3 FLOWER SIZE AND DISPLAY SIZE 7 2 4 NECTAR 7 2 5 SEXUAL SYSTEMS 7 2 6 FLOWERING PHENOLOGY 7 3 RELATIVE STRENGTHS OF POLLINATOR AND NON-POLLINATOR AGENTS OF SELECTION 7 3 1 A CASE STUDY OF RAPHANUS SATIVUS 7 4 SYNTHESIS OF ECOLOGICAL AND GENETIC OBSERVATIONS 7 5 COMMUNITY CONTEXT OF TRAIT EVOLUTION FLOWERING PHENOLOGIES OF ANIMAL-POLLINATED PLANTS: REPRODUCTIVE STRATEGIES AND AGENTS OF SELECTION 8 1 INTRODUCTION CONTENTS 8 2 COMPONENTS OF ?OWERING PHENOLOGIES 8 2 1 INDIVIDUAL PHENOLOGY 8 2 2 POPULATION PHENOLOGY 8 2 3 COMMUNITY PHENOLOGY 8 3 FLOWERING PHENOLOGIES AS REPRODUCTIVE STRATEGIES 8 3 1 ABIOTIC IN?UENCES ON PHENOLOGY 8 3 2 POLLINATION 8 3 3 HERBIVORY 8 3 4 SEED DISPERSAL AND GERMINATION 8 3 5 SEXUAL SYSTEM 8 3 6 LIMITS ON PHENOLOGICAL EVOLUTION 8 4 FLOWERING PHENOLOGY AND SELECTION ON PLANT REPRODUCTION: CASE STUDIES OF ALPINE PLANTS 8 4 1 FLOWERING-TIME EFFECTS ON POLLINATION SUCCESS AND SEED QUALITY 8 4 2 INTERSPECI?C COMPETITION FOR POLLINATION ALONG SNOWMELT GRADIENTS 8 4 3 METAPOPULATION STRUCTURE AND PHENOLOGICAL SEPARATION 8 5 CONCLUDING REMARKS FOR FUTURE RESEARCH FLOWER PERFORMANCE IN HUMAN-ALTERED HABITATS 9 1 INTRODUCTION 9 2 GENERAL EFFECTS OF DISTURBANCE AND THEIR REPRODUCTIVE CONSEQUENCES 9 3 EFFECTS OF HUMAN-CAUSED PERTURBATIONS ON PLANT ATTRIBUTES 9 4 EFFECTS OF HUMAN-CAUSED PERTURBATIONS ON POLLINATOR ATTRIBUTES 9 5 RELATION OF POLLINATION TO MODI?ED PLANT ATTRIBUTES 9 6 RELATION OF POLLINATION TO MODI?ED POLLINATOR ATTRIBUTES 9 7 RELATION OF PLANT REPRODUCTION TO MODI?ED POLLINATION 9 8 TRANSLATION INTO A PATH-ANALYSIS FRAMEWORK: AN EXAMPLE 9 9 MODULATORS OF PLANT REPRODUCTIVE RESPONSE 9 10 ANTHROPOGENIC DISTURBANCE AND THE STRUCTURE OF POLLINATION INTERACTION NETWORKS 9 11 PROSPECTS MATING STRATEGIES AND SEXUAL SYSTEMS REPRODUCTIVE ASSURANCE AND THE EVOLUTION OF UNIPARENTAL REPRODUCTION IN ?OWERING PLANTS 10 1 INTRODUCTION 10 2 REPRODUCTIVE ASSURANCE AND SELF-FERTILIZATION: THEORETICAL CONTEXT 10 3 REPRODUCTIVE ASSURANCE AND SELF-FERTILIZATION: EMPIRICAL APPROACHES 10 3 1 REPRODUCTIVE ASSURANCE AND THE EVOLUTION OF MIXED-MATING SYSTEMS 10 3 2 EXPLOITING INTRASPECI?C VARIATION TO TEST THE REPRODUCTIVE ASSURANCE HYPOTHESIS 10 4 ASEXUAL REPRODUCTION: A NEGLECTED MECHANISM OF REPRODUCTIVE ASSURANCE 10 4 1 CHALLENGES AND OPPORTUNITIES FOR INVESTIGATING THE EVOLUTION OF ASEXUALITY 10 5 MORE EXPERIMENTS NEEDED CONTENTS THE EVOLUTION OF SEPARATE SEXES: A FOCUS ON THE ECOLOGICAL CONTEXT 11 1 INTRODUCTION 11 2 THE GYNODIOECY PATHWAY TO DIOECY 11 2 1 HERMAPHRODITISM TO GYNODIOECY 11 2 2 GYNODIOECY TO DIOECY 11 2 3 PREDICTED RELATIONS OF FEMALE FREQUENCY AND KEY MODEL PARAMETERS 11 2 4 COMPARISONS OF OBSERVED AND PREDICTED FEMALE FREQUENCIES 11 3 IMPORTANCE OF ECOLOGICAL CONTEXT 11 3 1 HARSH ABIOTIC ENVIRONMENT 11 3 2 HARSH ENVIRONMENTS ALTER POLLINATION, POLLEN MOVEMENT, AND MATING SYSTEM 11 3 3 ENEMIES—ANALOGOUS TO HARSH ENVIRONMENTS? 11 3 4 MULTI-SPECIES INTERACTIONS AND LITTLE-STUDIED ASPECTS OF ECOLOGICAL CONTEXT 11 4 SPOTLIGHT ON UNRESOLVED ISSUES 11 4 1 SUBDIOECY: RE?ECTIVE OF CONSTRAINTS OR ADAPTATION? 11 4 2 POLLINATORS: FACILITATORS OR INHIBITORS OF SEXUAL-SYSTEM EVOLUTION? EFFECTS OF COLONIZATION AND METAPOPULATION DYNAMICS ON THE EVOLUTION OF PLANT SEXUAL SYSTEMS 12 1 INTRODUCTION 12 2 SINGLE-EVENT VERSUS RECURRENT COLONIZATION 12 3 EFFECTS OF SINGLE-EVENT COLONIZATION ON THE SEXUAL SYSTEM 12 3 1 LONG-DISTANCE DISPERSAL TO OCEANIC ISLANDS 12 3 2 LONG-DISTANCE DISPERSAL AND THE EVOLUTION OF DIOECY IN COTULA 12 4 EVOLUTION OF SEXUAL SYSTEMS IN A METAPOPULATION 12 5 EVOLUTION OF DOMINANT VERSUS RECESSIVE TRAITS IN A METAPOPULATION 12 6 MODES OF SEL?NG AND THE EVOLUTION OF GEITONOGAMY 12 6 1 MODEL OF GEITONOGAMY IN A METAPOPULATION 12 6 2 MODEL RESULTS AND DISCUSSION 12 7 CONCLUSIONS FLORAL DESIGN AND THE EVOLUTION OF ASYMMETRICAL MATING SYSTEMS 13 1 INTRODUCTION 13 2 THE EVOLUTION AND FUNCTIONAL BASIS OF ?ORAL AND SEXUAL-SYSTEM DIVERSITY 13 3 MATING IN MONOMORPHIC POPULATIONS 13 4 MATING IN DIMORPHIC POPULATIONS 13 4 1 EVOLUTION AND MAINTENANCE OF STIGMA-HEIGHT DIMORPHISM 13 4 2 ASYMMETRICAL MATING AND BIASED MORPH RATIOS 13 5 MATING IN TRIMORPHIC POPULATIONS 13 5 1 EVOLUTION OF MORPH RATIOS 13 5 2 VARIATION AND EVOLUTION OF SEXUAL ORGANS 13 6 DISCUSSION CONTENTS PART FLORAL DIVERSI?CATION ECOLOGICAL GENETICS OF ?ORAL EVOLUTION 14 1 INTRODUCTION 14 2 SIMPLE POLYMORPHISMS: ?ORAL COLOUR 14 3 ECOLOGICAL GENETICS OF QUANTITATIVE TRAITS 14 4 NATURAL SELECTION ON ?ORAL TRAITS 14 5 INDEPENDENT EVOLUTION OF CORRELATED TRAITS IN RADISH 14 5 1 MICROEVOLUTION 14 5 2 MACROEVOLUTION 14 6 FUTURE DIRECTIONS GEOGRAPHICAL CONTEXT OF ?ORAL EVOLUTION: TOWARDS AN IMPROVED RESEARCH PROGRAMME IN ?ORAL DIVERSI?CATION 15 1 INTRODUCTION 15 2 REPRESENTATION OF GEOGRAPHICAL VARIATION IN POLLINATION STUDIES 15 2 1 PATTERNS: HOW MUCH ATTENTION HAS GEOGRAPHICAL VARIATION IN PLANT TRAITS AND POLLINATORS RECEIVED? 15 2 2 PROCESSES: HOW MUCH DO WE KNOW ABOUT GEOGRAPHICAL VARIATION IN SELECTION ON POLLINATION-RELATED TRAITS? 15 3 OUTCOMES AND LIMITATIONS OF GEOGRAPHICALLY INFORMED STUDIES 15 3 1 OUTCOMES 15 3 2 LIMITATIONS AND A PROPOSAL 15 4 A CASE STUDY: CLINAL VARIATION OF LAVANDULA LATIFOLIA ?OWERS AND POLLINATORS 15 4 1 METHODS 15 4 2 STEP 1: CHARACTERIZE GEOGRAPHICAL VARIATION IN POLLINATORS 15 4 3 STEP 2: DEMONSTRATE POLLINATOR-MEDIATED SELECTION ON ?ORAL TRAITS 15 4 4 STEP 3: ASSESS GEOGRAPHICAL DIVERGENCE IN SELECTION 15 4 5 STEP 4: EVALUATE THE MATCH BETWEEN DIVERGENT SELECTION AND PHENOTYPIC DIVERGENCE 15 4 6 STEP 5: GENETIC BASIS OF POPULATION DIFFERENCES IN ?ORAL TRAITS 15 4 7 INTERPRETATION AND CAVEATS 15 5 CONCLUDING REMARKS: TOWARDS AN IMPROVED RESEARCH PROGRAMME IN ?ORAL DIVERSI?CATION POLLINATOR-DRIVEN SPECIATION IN PLANTS 16 1 INTRODUCTION 16 2 WHY ?OWERS EVOLVE 16 3 THE GEOGRAPHIC POLLINATOR MOSAIC 16 4 POLLINATION ECOTYPES 16 5 THE SCALE OF GENE ?OW IN PLANTS 16 6 GEOGRAPHIC MODES OF POLLINATOR-DRIVEN SPECIATION CONTENTS 16 7 IDENTIFYING POLLINATOR-DRIVEN SPECIATION 16 8 POLLINATORS AND REPRODUCTIVE ISOLATION 16 9 REINFORCEMENT OF ISOLATING BARRIERS 16 10 ADAPTIVE RADIATION 16 11 CONCLUSIONS FLORAL CHARACTERS AND SPECIES DIVERSI?CATION 17 1 INTRODUCTION 17 2 HOW MIGHT ?ORAL TRAITS AFFECT DIVERSI?CATION? 17 3 COMMON TESTS FOR KEY INNOVATIONS 17 4 METHODS 17 4 1 TRAIT DATASETS 17 4 2 ANALYSES 17 5 RESULTS 17 5 1 POLLINATION MODE 17 5 2 FLORAL SYMMETRY 17 5 3 FLORAL NECTAR SPURS 17 5 4 DIOECY 17 6 DISCUSSION FLORAL BIOLOGY OF HYBRID ZONES 18 1 INTRODUCTION 18 2 GENETIC ARCHITECTURE OF SPECIES DIFFERENCES; WHAT DO HYBRID ?OWERS LOOK LIKE? 18 3 FLORAL TRAITS AND THE FREQUENCY OF MATING BETWEEN SPECIES AND HYBRIDS 18 3 1 ETHOLOGICAL ISOLATION 18 3 2 MECHANICAL ISOLATION 18 4 THE RELATIVE IMPORTANCE OF ETHOLOGICAL AND MECHANICAL ISOLATION 18 4 1 FLORAL TRAITS IN IPOMOPSIS AGGREGATA AND I TENUITUBA AND POLLINATOR BEHAVIOUR 18 4 2 SIMULATION MODEL OF ETHOLOGICAL AND MECHANICAL ISOLATION 18 4 3 GEOGRAPHICAL VARIATION IN PRE-MATING ISOLATION 18 5 POST-MATING ISOLATION 18 6 FLORAL TRAITS AND THE ?TNESS OF HYBRIDS 18 7 CONCLUSIONS AND FUTURE DIRECTIONS