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博士論文 Evolutionary History, Species Diversity and Biogeography of Amphidromous Neritid Gastropods in the Indo-West Pacifi

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博士論文 Evolutionary History, Species Diversity and Biogeography of Amphidromous Neritid Gastropods in the Indo-West Pacifi 博士論文 Evolutionary history, species diversity and biogeography of amphidromous neritid gastropods in the Indo-West Pacific （インド・西太平洋域における両側回遊性アマオブネ科腹足類の 進化史および種多様性と生物地理に関する研究） 福森 啓晶 平成 25 年度 博士学位論文 Evolutionary history, species diversity and biogeography of amphidromous neritid gastropods in the Indo-West Pacific （インド・西太平洋域における両側回遊性アマオブネ科腹足類の 進化史および種多様性と生物地理に関する研究） Global Marine Environment Graduate school of frontier sciences The University of Tokyo 東京大学大学院 新領域創成科学研究科 自然環境学専攻 地球海洋環境学分野 福森 啓晶 Hiroaki Fukumori Contents Chapter1: General Introduction 1-1: Amphidromy in tropical and subtropical freshwater fauna 1 1-2: Neritidae as a model group for understanding tropical stream ecosystems 5 1-3: Origin and evolution of amphidromous taxa 6 1-4: Morphology, ecology and evolution of planktotrophic larvae 7 1-5: Species and population diversity, taxonomy and biogeography 8 1-6: Aim, scope and outline of thesis 10 Table 1-1 11 Figure 1-1 12 Chapter 2: Molecular phylogeny of the superfamily Neritoidea (Gastropoda: Neritimorpha) 2-1: Introduction 13 2-2: Materials and Methods Taxonomic sampling 16 DNA extraction, amplification and sequencing 17 Sequence analysis and phylogenetic reconstruction 18 Divergence time estimates 20 Ancestral character-state reconstruction of ecological and morphological traits 21 2-3: Results Sequence data 22 Phylogenetic analyses 23 Divergence time estimates 26 Ancestral character-state reconstruction 27 2-4: Discussion Phylogeny and classification of Neritoidea 28 i Habitat shifts, evolution of amphidromy and reinvasion of the sea 32 Parallel evolution of limpet form in stream environment 34 Origins of benthic development 35 Table 2-1 to 2-3 39–42 Figure 2-1 to 2-11 43–53 Chapter 3: Evolutionary ecology of settlement size in planktotrophic neritimorph gastropods 3-1: Introduction 54 3-2: Materials and Methods Selection of study taxa 58 Measurement of opercular nucleus 58 Comparison between sizes of opercular nucleus and protoconch 59 Comparison of settlement size distribution among lineages and habitats 59 Relationship between settlement size and geographic range 60 Statistical analyses 60 3-3: Results Size of opercular nucleus 61 Size of protoconch 62 Comparison of settlement size distribution among lineages and habitats 64 Comparison of settlement size and geographic range 64 3-4: Discussion Inference of settlement size from measurement of adult operculum 65 Settlement size as an identification trait for juveniles and larvae 66 Phylogenetic constraints on settlement size for neritimorph subclades 67 Adaptive significance of smaller settlement size for amphidromous taxa 69 Settlement size and geographic distribution range 73 Concluding remarks 74 Table 3-1 to 3-3 76–81 Figure 3-1 to 3-6 82–87 ii Chapter 4: Taxonomy and biogeography of the amphidromous Neritidae in the Indo-West Pacific 4-1: Introduction 88 4-2: Materials and Methods Taxonomic sampling and selection of specimens for DNA sequencing 92 DNA extraction, amplification and sequencing 93 Sequence analysis and phylogenetic reconstruction 94 Species recognition and assignment of scientific names 95 Genetic and geographic distances 96 Biogeographic patterns of limnic neritids 97 4-3: Results Sequence data 98 Comparison of genetic distances between and within species 99 Relationship between genetic and geographic distances 100 Biogeographic patterns of limnic neritid species 100 4-4: Discussion Recognition of biological species in limnic Neritidae 103 Assignment of valid names to biological species 106 Dispersal ability of amphidromous neritids 107 Biogeographic patterns of species richness 110 Air temperature: limiting factor in the present and past 112 Table 4-1 to 4-2 114–120 Figure 4-1 to 4-11 121–139 Chapter 5: General Disscussion 5-1: Formation and maintenance mechanisms of island stream fauna 140 5-2: Contributions to taxonomy and conservation of limnic neritids 144 5-3: Future perspectives 146 Acknowledgements 149 References 152 iii Appendix 1: Specimens of limnic Neritidae from Indo-West Pacific used for species taxonomy and DNA sequencing in Chapter 4 Appendix 2: Type specimen catalog of limnic Neritidae used for species taxonomy in Chapter 4 iv Chapter 1: General Introduction 1-1: Amphidromy in tropical and subtropical freshwater fauna Island biodiversity has been a major topic of debate in evolutionary ecology and conservation biology. Islands generally form unique ecosystems because they are isolated from other islands and continents (Grant 1998). With such patchy and fragmented conditions, the role of immigration and extinction in relation to area size and proximity to source areas has been elaborated in the theory of island biogeography (MacArthur & Wilson 1963, 1967; Locos & Schluter 2000; Emelson & Kolm 2005). When an island is colonized by dispersal from other islands and continents, the physical and genetic separation of populations often leads to an important evolutionary consequence—speciation (Mayr 1970; Turelli et al. 2001; Thorpe et al. 2008). The speciation process due to geographic isolation is further promoted by the founder effect (Comes et al. 2008). Adaptive radiation and speciation may also occur on isolated islands with unoccupied niches (Grant 1998). Island fauna and flora thus tend to be unique, but many endemic and locally adapted species occupy limited geographic areas and have small population sizes and specific habitat requirements. Island biodiversity is now being threatened by human activities including habitat destruction and introduction of invasive species, which have resulted in local or global extinction and consequently a loss of ecological stability (Whittaker & Fernández-Palacios 2007). In tropical and subtropical regions worldwide, numerous continental and oceanic islands exist and many such islands have freshwater streams (Falkland 1991). In general, island streams are smaller than continental rivers, having relatively high gradients and short distances from headwaters to stream mouth (McDowall 2007). Such streams are too short, thus in the tropics they become raging torrents during the rainy season, while during drought 1 they may be dried up (McDowall 2007; Kano et al. 2011). These environmental conditions present a serious problem for primary freshwater animals that spend the whole lives in streams and rivers, even if they could somehow colonize the islands by rare, stochastic dispersal events (Strong et al. 2008; McDowall 2010). Amphidromous animals, on the other hand, flourish in the streams of tropical and subtropical islands (McDowall 2010; Kano et al. 2011). Amphydromy or amphidromous life cycle has been defined by McDowall (2010) as follows: (1) spawning occurs in freshwater, where egg development also takes place; (2) hatched larvae are immediately transported to sea in the flows of streams; (3) they spend a few weeks to a few months at sea, feeding and growing; (4) there is a return migration to freshwater by small post-larvae to well-grown juveniles; (5) they then mature and spawn, thus completing the cycle. Since the introduction of the term as a subcategory of diadromy by Myers (1949), this life cycle has been found in many different animal lineages (Table 1-1), such as fishes (e.g. Gobiidae, Eleotridae and Plecoglossidae), crustaceans (e.g. Atyidae and Palaemonidae) and gastropod molluscs (Neritidae, Neritiliidae, Stenothyridae, Thiaridae and Acochlididae; Fig. 1-1). Most amphidromous animals are microalgal herbivores, feeding on stream periphyton (e.g. McDowall 2007; Bauer 2011; Kano et al. 2011). The intensities of competition as well as predation in upstream freshwater environments may be lower than in most marine environments; this is particularly the case on islands due to the inaccessibility for non-diadromous competitors and predators (Holthuis 1995; McDowall 2010). The short and steep conditions of the island streams are also favorable for the amphidromous animals. These conditions provide easier access of amphidromous larvae to the ocean and easier access of settled juveniles to upper streams. The females of most amphidromous species reproduce a larger number of smaller eggs than those of non-diadromous, direct developing species do (McDowall 2010; Kano et al. 2011; Bauer 2011). These reproductive traits, known as r-strategy, involve a greater risk of offspring mortality than the so-called K-strategy of direct developers but often give an 2 advantage in heterogeneous or unstable environments (e.g. Strathmann 1985). The rate of larval transport to new habitats can be significantly enhanced by the presence of such numerous larvae. Also, the hatched larvae of amphidromous species have a planktotrophic stage that enables exploitation of the trophic riches of the marine phytoplankton during the long pelagic life (McDowall 2007). The mechanisms of amphidromy thus allow larval dispersal and (re)colonization of streams in remote islands, where habitats may be ephemeral and there is a risk of local extirpation (McDowall 2010). Correspondingly, recent studies have revealed low genetic variations among distant populations (Bebler & Foltz 2004; Cook et al. 2006; Hoareau et al. 2007; Crandall et al. 2010; Castelin et al. 2013). For instance, two species of amphidromous neritid gastropods show high gene flow over several thousands of kilometers among South Pacific archipelagos (Crandall et al. 2010). An amphidromous prawn Macrobrachium lar similarly reveals a low level of genetic structure across the West Pacific and between Indian and Pacific Ocean basins (Castelin et al. 2013). For
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