化學受器是昆蟲主要的感覺器官，昆蟲利用嗅覺來感知食物、配偶、宿主、掠食者等外在因子。榕小蜂科的物種丟失了大多數的化學受器基因，可能與其封閉的特殊生活史有關。即使如此，榕小蜂的嗅覺在其與榕樹的互利共生關係中至關重要，榕小蜂主要透過辨識榕樹隱頭果氣味，來達到專一性授粉。本論文透過定序兩種榕小蜂的基因體跟轉錄體，研究小蜂的化學受器基因如何與其宿主共演化。本文第一章使用粒線體基因標記，進行系統發生以及族群遺傳分析，進而釐清兩研究物種Wiebesia pumilae, W. sp3和他們的近親W. sp1之間的親緣關係、天然分佈位置、自然宿主，並揭露W. sp3有數個族群源於人為引入，且在其入侵地發生多次獨立轉換宿主，由原本共生的愛玉 (Ficus pumila var. awkeotsang)轉至薜荔 (Ficus pumila var. pumila)。經由回顧前人在入侵族群做的物候調查，我提出一個可能機轉解釋榕小蜂的宿主轉換在不同榕樹性別系統之最終演化結果。本文第二章提供詳細的生物資訊流程描述組裝及注釋兩研究物種的基因體以及粒線體基因體，並進行種間基因演化速率分析。
本文第三章探討不同演化層面和尺度下，榕小蜂嗅覺基因與其宿主的共演化。在精細演化尺度，利用近期與宿主達成共演化的W. pumilae和W. sp3的基因體與轉錄體，發現在科內基因拷貝數保守的嗅覺基因出現種間差異表達現象。而在跨越整個榕小蜂科的廣大演化尺度，藉由比較W. pumilae、W. sp3和Ceratosolen solmsi三物種，發現在嗅覺受器 (olfactory receptor)出現各支系獨有的適應性基因串聯重複 (adaptive tandem gene duplication)，極有可能是與宿主榕樹氣味長期共適應、共演化的結果。最後我比較與不同性別系統榕樹共生之榕小蜂，發現三個在榕小蜂科中出現縮減的嗅覺基因家族，於雌雄同株榕樹的小蜂Elisabethiella stueckenbergi都出現較多的基因數目擴張，可能與雌雄同株榕樹小蜂具有更頻繁的宿主轉換有關。

Pollinating fig wasps (Agaonidae) have one of the most reduced chemosensory genes in insects, which is probably associated with specialized life cycle in obligate mutualism. On the other hand, olfaction plays a crucial role in maintaining host specificity in the fig-fig wasp coevolution. In this thesis, I sequenced genomic and transcriptomic data from two fig wasp species to understand how reduced chemosensory genes maintain host-specificity during species divergence. The first chapter describes the evolutionary relationships of the two studied fig wasps (Wiebesia pumilae and W. sp3), their close species (W. sp1), and their associated hosts (Ficus pumila var. pumila and Ficus pumila var. awkeotsang), which revealed that while originally an endemic species, recent human intervention had resulted in introduced populations along with recurrent host-shifting in W. sp3. Possible mechanism for distinct co-pollinator pattern seen in different fig sexual systems was also proposed. The second chapter provides bioinformatics pipelines to generate high quality nuclear genomes and mitochondrial genomes of both species using next generation sequencing, and assess the evolutionary rates in protein-coding genes between them.
The final chapter characterizes chemosensory gene evolution of fig wasp from multiple evolutionary perspectives. For fine scale evolution, utilizing the genome and transcriptome of W. sp3 and W. pumilae, both of which codiverged recently with their host, I discovered that regulatory changes at copy-number conservative chemosensory genes are associated with local coadaptations. For large scale evolution, by comparing the two Wiebesia species with Ceratosolen solmsi, I found that lineage-specific adaptive tandem gene duplications in olfactory receptors (OR) family may drive phenotypic coevolution with figs. For olfactory evolution in wasps belonging to different sexual systems of hosts, larger expanded gene families were found in the ancestrally contracted gene families: OR, gustatory receptor (GR) and odorant-binding protein (OBP) in the monoecious fig wasp Elisabethiella stueckenbergi, possibly reflecting differences in host-shifting frequency.

口試委員會審定書 #
誌謝 i
中文摘要 ii
ABSTRACT iii
CONTENTS v
LIST OF FIGURES ix
LIST OF TABLES xi
Chapter 1 Genetic evidence revealed pollinator sharing via host-switching in pollinators associated with Ficus pumila 1
1.1 Introduction 1
1.2 Material and Methods 2
1.2.1 Phylogeny and population genetics 2
1.2.2 Species distribution modeling 3
1.3 Results 4
1.4 Discussion 6
1.4.1 How the introduced fig wasp species affect fig-fig wasp mutualism? 7
1.4.2 Evolutionary outcome of co-pollinator caused by host shifting 8
Chapter 2 The nuclear and mitochondrial genome of Wiebesia sp3 and Wiebesia pumilae 9
2.1 Introduction 9
2.1.1 Applying genomics in fig wasp study 9
2.1.2 Study species and system 10
2.2 Material and Methods 12
2.2.1 Biological materials for genomic DNA sequencing 12
2.2.2 Biological materials for RNA sequencing 13
2.2.3 Library construction and sequencing 13
2.2.4 Sequencing quality check 13
2.2.5 Taxonomic validation 14
2.2.6 Read decontamination and de novo assembly of jelly-fig wasp 14
2.2.7 Mapping-based assembly of creeping-fig wasp 16
2.2.8 Repeat annotation 17
2.2.9 Gene prediction 17
2.2.10 Manual gene curation 18
2.2.11 Functional annotation 19
2.2.12 Manual annotation of interested genes 19
2.2.13 Mitochondrial genome assembly and annotation 20
2.2.14 Orthology 21
2.2.15 Evolutionary rates between Wiebesia species 21
2.3 Results 22
2.3.1 Sequencing quality check and validation of taxonomy 22
2.3.2 Blobtools and de novo assembly of jelly-fig wasp 22
2.3.3 Genome assembly of creeping-fig wasp 23
2.3.4 Repeat annotations and Gene predictions 24
2.3.5 Functional annotation 24
2.3.6 Mitochondrial genome 24
2.3.7 Orthology 25
2.3.8 Evolutionary rate between Wiebesia species 25
2.4 Discussion 25
2.4.1 de novo genome assembly and symbionts DNA removal 25
2.4.2 Genome assembly using a closely related reference 27
2.4.3 Reference-based RNA assembly 28
2.4.4 Performance of ab initio predictors 29
2.4.5 Quality of gene predications 29
2.4.6 Mitochondrial genome assembly 29
2.4.7 Gene rearrangements in mitochondrial genome 30
2.4.8 Evolutionary rate between two species 30
2.4.9 Mito-nuclear coevolution 31
2.4.10 Rapid evolution and changes of expression in protease genes 32
Chapter 3 The evolution of chemosensory genes in pollinating fig wasps 34
3.1 Introduction 34
3.1.1 Basis of host recognition in pollinating fig wasps 34
3.1.2 Study system and design 35
3.2 Material and Methods 37
3.2.1 Sample collection and RNA sequencing 37
3.2.2 de novo transcriptome assembly of E. stueckenbergi 37
3.2.3 Reconstruction of fig wasp phylogeny 38
3.2.4 Annotation of chemosensory genes 38
3.2.5 Phylogenetic analysis of chemosensory genes 39
3.2.6 Selection analysis 39
3.2.7 Localization of transposable elements and odorant receptors within jelly fig wasp genome 40
3.2.8 Cross-species differential expression analysis on two Wiebesia species 41
3.3 Results 42
3.3.1 de novo transcriptome assembly 42
3.3.2 Phylogeny of studied fig wasps 42
3.3.3 Evolution of chemosensory gene families in fig wasps 42
3.3.4 TE density and gene duplication in OR 43
3.3.5 Cross species differential expression analysis 44
3.4 Discussion 44
3.4.1 On the fine-scale evolution between jelly-fig and creeping-fig wasp 45
3.4.2 Long-term effects of co-cladogenesis 46
3.4.3 Host sexual system and sizes of chemosensory gene family 48
Chapter 4 Conclusion 49
REFERENCE 50
FIGURES 72
TABLES 95

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