GENERAL INTRODUCTION - 生態學與演化生物學研究所

3 General introduction:

The current distribution of species is the consequence of past events that have considerably changed the environment. During the Last Glacial Maximum, the size of the continents was greater, the geography and the climate were quite different from today. Changes occurred shaping the current world. Species ranges expanded, and retracted leading to the distributions we observe today. Analysis of the spatial structure of genetic diversity has permitted, for example, inference of pathways of colonization, such as the tracks of post-glacial expansion of many species from refugia after the Last Glacial Maximum (Hewitt, 2004; Muellner et al., 2005) or inference of inter-continental plant migrations (Dick et al., 2007; Erkens et al., 2009;

Muellner et al., 2006). However in some regions of the world, the history of the latest expansions is unclear. For example in Australasia, numerous studies have tried to delimit biological regions and limits for the floras and the faunas, such as the Wallace line, but the limits are still debated today as they are species dependent (Cox, 2001;

Esselstyn et al., 2010; van Welzen et al., 2011). Southeast Asia is at the center of these debates, firstly because of the incredible biodiversity of these regions (Myers, 2000) and secondly the diversity is specific to certain areas such as Japan, or the Philippines.

In this region, contact zones between different biogeographic provinces may provide a unique key to determine patterns of species occurrence and distribution. Indeed, what preserves the identities of biotas in contact zones between long-separated floras and faunas? Do competition and pre-emption of space limit the spread of ecologically redundant species into the other biota? In this prospective, Taiwan presents a fascinating opportunity to analyse ecological and evolutionary processes in sites of

active biotic exchange: it is a recent contact zone [less than 2.5 million years old (Malavieille et al., 2002)] between two different biotas. It formed as a totally new island, which may have been connected to the mainland but if so, only at glacial maxima. Its biogeographic neighbours are the Asian continent and the Philippines, an old isolated group of islands that has never been part of a continent (Sibuet and Hsu 2004). This allows monitoring how two floras and faunas may mix. Hence Taiwan is a model system to investigate processes occurring during the early stages of such contacts. The situation is thus also of relevance to questions about biological invasion, an important aspect of contemporary global change.

Figure 1: The geographic situation of Taiwan. From the map it is apparent that Taiwan can be colonised from the continent and from the Philippines. The link between the Philippines and New Guinea over the Moluccas is also conspicuous. A continental plateau with shallow waters is joining Borneo, Java, Sumatra and the Asian mainland and forms Sundaland. The waters separating Borneo from the Philippines are much deeper, so that the latter islands were never in contact with Sundaland (Heaney et al. 2005). Hence during warm climatic episodes, a moist tropical flora could have colonised Taiwan from the Philippines, but also from the Indochinese peninsula.

Moreover Taiwan is a relatively small island. Islands are generally depauperate in species relative to mainland regions, yet they are home to some of nature’s most striking adaptive radiations. The low species richness of islands can be attributed both to their limited size, which increases extinction rates, and to their isolation (MacArthur and Wilson 1967). At the same time, some clades present substantial ecological and phenotypic diversity on islands, a diversification which probably results from evolutionary radiation into empty niches associated with low species numbers (Algar and Losos, 2011) in agreement with the ecological theory of adaptive radiation (Schluter, 2000). Investigating early stages of small island colonization by highly dispersive species may allow to detect early phases of ecological niches expansion and specialization into these ecological niches, a process that could lead to speciation.

Taiwan is a unique territory in Asia. With a high rate of endemism, the Taiwan flora displays a surprising mix of the Philippines and Chinese floras (Hsieh, 2002). These two floras are most different. Indeed numerous authors have tried to analyze the specificities of the Philippine flora (Simpson, 1977). The past links with the continent (including Japanese Islands) have been highlighted in the studies of closely related species such as Cunninghamia konishii which is directly derived from its continental sister species C. lanceolata (Lu et al., 2001; Hwang et al., 2003; Chung et al., 2004), similarly with Lilium formosanum and the Japanese L. longiflorum (Hiramatsu et al., 2001) or again for Rhododendron species (Brown et al., 2006; Chung et al., 2007). At the species level, Taiwan species display important local differentiation from the populations of the areas of origin (Chiang et al., 2001; Huang et al., 2002; Huang et al., 2004; Cheng et al., 2005; Huang and Lin, 2006). In Taiwan, the Central Mountain Range (CMR over 2,000m high) represents an insurmountable barrier for plant

species (Lin, 2001; Huang et al., 2002; Cheng et al., 2005) but few studies have described the effect of the latitude on the genetic structure. Indeed the island of Taiwan is a subtropical territory (Yen and Chen, 2000; Chen et al., 2005): while in the north the climate is cold, but no frost at sea level, the southern part of Taiwan is warmer with one yearly rainy season. Studies have shown either no population structuring throughout Taiwan (Chung et al., 2004; Cheng et al., 2005; Wu et al., 2006; Shih et al., 2007) or north-south structuring of the populations, a feature which has always been attributed to post glaciations expansion from refugia for plants (Huang et al., 2004; Cheng et al., 2005; Liao et al., 2010) as well as for terrestrial mammals (Yuan et al., 2006). Nevertheless for Cyclobalanopsis glauca (tropical affinity), the inferred refuge location was located in the Southeast of Taiwan (Huang et al., 2002) while the inferred refuge location for Trochodendron aralioides (temperate affinity) is in the North of Taiwan (Huang et al., 2004).

To go further in our understanding on the current biogeographic patterns of species and on community diversity, we decided to study a group of interacting organisms that has become a model system in community ecology: figs, their specific pollinators and associated insect communities (Herre et al. 2008).

Fig trees belong to genus Ficus. With about 800 species worldwide, this is the most speciose tree genus (Berg, 1989). There are 26 Ficus taxa in Taiwan. Their distribution areas have been established recently (Tzeng, 2004). The fig trees in Taiwan present a suite of more or less unique characters. First, as opposed to other plant genera in Taiwan (Hsieh, 2002), there are only few endemic species (two endemics, for 26 taxa). Second, many of the Taiwanese Ficus have widespread distributions. An excess of widespread species is actually an excess of species with

strong dispersal capacity. These special characters (few endemic species and an important number of widely distributed species) support the hypothesis that Taiwan is a territory recently open to colonization by plants, a situation which is quite different from other well-studied old island such as New Caledonia, although colonisation is more recent than previously asumed (Grandcolas et al., 2008) and which present 76%

endemic plant species (Jaffre et al., 1998). Finally, the non-endemic Ficus of Taiwan may originate from two sources: the continent (including Japan) and the Philippines Archipelago. Of the 26 fig species, only five occur both on the Asian continent and the Philippines. Comparatively to the global tropical plant flora of Taiwan which includes a number of species present both in the Philippines and on the continent (Hsieh, 2002), the fig tree flora is clearly separated in two entities (Table 1). It is important to note that even some species of tropical origin thrive in northern Taiwan (e.g. Ficus septica, F. benguetensis and F. variegata) and some more temperate species thrive in the subtropical part of Taiwan in the south (e.g. Ficus erecta var.

beecheyana and F. subpisocarpa). To summarize, the Ficus flora of Taiwan is a mixture of the Philippine and continental Asia species. They present mainly tropical climate affinity. Ficus is the only ubiquitously locally diverse genus in tropical lowland rainforest and this is achieved by a large portion of the regional pool of species being present locally (Harrison, 2005). However on islands, diversity may be reduced. This is the case in Taiwan. For instance there are only four species of monoecious hemiepiphytic Ficus species in Taiwan (Corner, 1965). Of these two belong to section Conosycea (Ficus microcarpa and F. benjamina var. bracteata) and two belong to section Urostigma (F. subpisocarpa and F. caulocarpa).

Table 1: Complete list of Ficus species recorded in Taiwan, and the continental provinces of Fujian and Guangdong. Presence of these species on the Asian mainland, RyuKyu and the Philippines is indicated. For presence in Taiwan, Orchid Island is indicated when the species does not occur on the main island of Taiwan but only on Orchid Island.

Species are numbered according to Corner’s (1965) checklist and named according to the latest publications (Berg and Corner, 2005).

Asian mainland

Guangdong Fujian Taiwan Philippines RyuKyu

Subgenus Urostigma

F. sinociliata (species incerta sedis) X X F. undulata (species incerta sedis) X X

170. F. tannoensis N X (SE)

9 Table 1: continued

Asian mainland

Guangdong Fujian Taiwan Philippines RyuKyu

Subgenus Synoecia 19 sp 5 sp 3 sp 5 sp 13 sp 2 sp

Moreover, Ficus are part of an obligate pollination mutualism. Due to the closed urn-shaped inflorescence and a very important number of available ovules (to feed the pollinator’s larva), the pollination of figs depends on obligatory and specific pollinating wasps (Hymenoptera, Agaonidae sensu Cruaud et al., 2010). Together they are the actors of an obligate and specific mutualistic relationship with special co-adaptations. The specific fig-fig wasp mutualism seems to follow locally the one-to-one rule (one-to-one Agaonidae species for one-to-one Ficus species). This idea was basically established by Janzen in 1979 but recent studies have shown a trend that Ficus could often have more than one pollinator species (Lopez-Vaamonde et al., 2001; Cook and Rasplus 2003; Molbo et al., 2003; Machado et al., 2005; Haine et al., 2006; Lin et al., 2011; Moe et al., 2011; Cornille et al. in press). Nevertheless, the fig and fig wasp association remains highly specific (Jousselin et al., 2008). The female pollinator has to find the receptive fig (Phase B sensu Galil and Eisikowitch, 1969 and Figure 2) in the middle of the vegetation. At the receptivity phase, the figs emit volatiles compounds to attract the pollinators (Grison-Pigé et al., 2002; Proffit et al., 2008;

Hossaert-McKey et al. 2010). The insects will approach preferentially the odor of its host tree. Proffit et al. (2008) show that the fig trees produce specific bouquets of odors different among species; nevertheless, it is important to note that the variation among trees of the same species is important, too.

Beyond the pollinating wasps, a whole community of specific chalcidoid wasps (Hymenoptera, Chalcidoidea) also develops within the figs. These non-pollinating fig wasps (NPFW) species are poorly known in Taiwan as in other parts of the world except Africa (van Noort and Rasplus, 1997). Only one complete study has been done on Ficus microcarpa (Chen et al., 1999) establishing the presence of 20 species.

These species are external parasites: they oviposit through the fig wall to reach the

ovules they aim to parasitize. When their ovipositor is inside the fig, the NPFW are exceptionally vulnerable to predators. Former studies have shown that ants may thrive in fig trees, feeding on NPFW (Schatz et al., 2006). Pollinating wasps are also predated by ants living on fig trees in the tropics (Schatz et al., 2008) and in temperate areas (Schatz and Hossaert-McKey, 2003). Ants may be numerous on fig trees in the tropics (Schatz et al., 2008; Bain, pers. obs.) but their presence is poorly documented.

With the exception of the work by Schatz, there have been few studies on ant-fig trees interactions. Some studies have investigated ant-Hemipteran interactions on figs (Compton and Robertson, 1988; Dejean et al., 1997; Cushman et al., 1998) and a study has shown that Ficus pisifera (also known as F. obscura var. borneensis; Berg and Corner, 2005) is a myrmecophytic plant (Maschwitz et al., 1994). The path followed by ants to colonise Taiwan is unknown. We may wonder if the strong associations with ants which sometimes prevail in the tropics have reached as far north as Taiwan as associations with ants seem to become less strong outside the tropics.

Using this quite unique model system in community ecology, the main objectives of the present work was to analyse colonisation patterns of this recent island, starting by the fig species. This will be the first step in our understanding of the origins and subsequent evolution of community structure and functioning of interacting species.

In order to perform such studies we selected sufficiently abundant species that include species that have most probably colonized Taiwan from the continent, and species that have colonized Taiwan from the Philippines.

0 10 20 30 40 50 60

Apocrypta Sycophaga

Sycophila

Platyneura

Sycoscapter Platyneura

Inquiline - parasite Gall-maker

Fig Diameter (mm)

Pre-receptive Receptive ---Post-receptive--- Maturity Pollinator

Figure 3: The five phases of Ficus erecta var. beecheyana fig development. Prereceptive figs (A phase) are greenish, the ostiole is tightly closed. At the beginning of the receptivity period (B phase), the ostiole becomes looser, allowing female pollinating wasps to enter inside the fig. The longest phase is the interfloral phase (C phase). The figs are hard and have lost their shine and the ostiole is tightly closed. Here birds have peaked at the C phase fig.

During the wasp emergence phase for male figs (D phase) and the final ripening stage for female figs (E phase), the figs swell and become soft. Male D phase figs become brownish yellow, while female figs become purplish white to dark purple.

Ficus erecta Thunb. (Figure 3) belongs to section Ficus of subgenus Ficus. It is a dioecious shrub or a treelet and is found in Japan, Korea, Ryukyu Islands, and in continental China as far north as Jiangsu and inland to Yunnan. It is thus a species adapted to cold conditions (for a Ficus species) with a marked winter. Two varieties and two forms were retained by Corner (1965). The variety occurring in Taiwan is beecheyana (Hook. et Art.) King and the variety erecta on the continent.

14 Figure 4: Ficus variegata figs.

Ficus variegata Blume (Figure 4) belongs to subgenus Sycomorus section Sycomorus, subsection Neomorphe. It grows, often as a pioneer, into a large free standing dioecious tree. The species is extremely widespread, from China to Northern Australia (Queensland). In China it is present from south Yunnan to Fujian. Thus it reaches even less far north than F. subpisocarpa but it occurs further inland. It could have colonized Taiwan either from the Philippines or from the continent.

Figure 5: Ficus subpisocarpa figs. Ficus subpisocarpa is monoecious and cauliflorous. The figs grow on the branches and trunk, with strong synchrony.

Ficus subpisocarpa Gagnep. (Figure 5) belongs to subgenus Urostigma, section Urostigma, subsection Urotigma. It is a relatively small monoecious hemiepiphyte often growing on rocks. It is found in Southern Japan, Eastern continental China (northern limit, south east Zhejiang), Taiwan, Vietnam, Cambodia, Northeast Thailand and might be present in the Mollucas (Eastern Indonesia archipelago) (Berg et al., 2011)). Hence it is a species that thrives in relatively cool climates along the seacoast, but it is not found in the colder climates and at high altitudes where Ficus

erecta var. beecheyana can occur. Moreover it is often observed in urban environments.

Figure 6: The five phases of Ficus septica fig development. Prereceptive figs (A phase) are light green and shiny, the ostiole is tightly closed. At the beginning of the receptivity period (B phase), the ostiole becomes looser, allowing female pollinating wasps to enter inside the fig. The longest phase is the interfloral phase (C phase). The figs are hard and have lost their shine and the ostiole is tightly closed. During the wasp emergence phase for male figs (D phase) and the final ripening stage for female figs (E phase), the figs swell and become soft.

Their color changes to greenish yellow. Nevertheless while D phase male figs characteristics are very similar with those of C phase figs, E phase female figs keep swelling and finally burst open.

Ficus septica Burm.f. (Figure 6) belongs to section Sycocarpus of subgenus Sycomorus. It is usually a small dioecious tree but may reach 25m. It is common from the Ryukyu Islands and Taiwan to the Vanuatu and throughout the islands of Malesia, but it is absent from continental Asia. As such it is a species of equatorial and tropical distribution, and Taiwan represents an extreme in its distribution.

Figure 7: The Ficus benguetensis figs. This species grows figs in cluster on the trunk of by pair on the branches. Often ants are living between the figs and the trunk inside the clusters.

The E phase female figs burst open as F. septica figs.

Ficus benguetensis Merr. (Figure 7) also belongs to section Sycocarpus of subgenus Sycomorus. It is a dioecious shrub of tree up to 15 m tall. It is limited to the Ryukyu Islands, Taiwan and the Philippines. According to Berg (2011) it belongs to the species group of F. ixoroides (Borneo), F. lepicarpa (Malesia in general) and F.

ternatana (Moluccas) and is hence not closely related to F. septica.

Figure 8: The five phases of Ficus pedunculosa var. mearnsii fig development. A phase figs are greenish purple and shiny. The receptive figs are hairy and still greenish purple. At the beginning of the C phase, the ostiole becomes very tight. The final phases of fig development are very similar in male and female figs: they become dark purple.

Ficus pedunculosa Miq. var. mearnsii (Merr.) Corner (Figure 8) belongs to subgenus Ficus section Ficus subsection Frutescentia. The distribution of F. pedunculosa extends from Taiwan to New Guinea. It has very large seeds for a Ficus and belongs to a group of species including other species with very large seeds such as F.

deltoidea, which is either epiphytic or grows on very poor sandy soil (e.g. var.

arenaria), and indeed F. pedunculosa var. pedunculosa lives on harsh rocky environments (Bain, pers. obs.). This suggests that the affinity of the species is rather with the Malesian species of subsection Frutescentia, i.e. it belongs to an equatorial group. The form present in Taiwan is var. mearnsii. It is a prostrate shrub on sea-coasts and mountains, but in Taiwan it is absent on mountains. The variety is to be

observed in Luzon (Philippines) and in the islands stretching from Luzon to the main island of Taiwan (Babuyan and Batanes Islands, Orchid Island).

Figure 9: The five phases of Ficus tinctoria subsp. swinhoei fig development. Pre-receptive figs are green to brownish green. Receptive figs are greenish yellow, the ostiole is shinny and darker. At the beginning of the interfloral phase (C phase), the ostiole becomes tightly closed and the fig color gets darker. The final phase of the fig development is very different between male and female figs: male figs become yellow and swollen while the female figs become red to purple and are less swollen.

Ficus tinctoria G. Forst. subsp. swinhoei (King) Corner (Figure 9) belongs to subgenus Sycidium, section Palaeomorphe (Berg and Corner, 2005), a section that includes all the hemiepiphytic species of dioecious Ficus. Subspecies swinhoei is a scandent shrub on rocks and in Taiwan it is mainly restricted to sea-shores. It is also found in Mindanao. Berg and Corner (2005) included the subspecies within F.

tinctoria subspecies tinctoria, i.e. within the subspecies of equatorial distribution. On the Asian continent the form present is subspecies gibbosa. Hence subspecies swinhoei has an equatorial affinity.

In order to provide a comparative analysis of the genetic structure of the fig species present in Taiwan throughout their range, we had to develop a unique set of genetic markers that would be portable among any Ficus species on a worldwide basis. We developed a set of 20 highly portable microsatellite primers. The markers were both easy to amplify, and easy to read in 24 Ficus species from the six subgenera occurring in Taiwan. (article 1). This will facilitate our investigation of the genetic structure of complete regional floras using a single set of marker.

During the period allotted to this thesis we were able to examine the following questions :

1) What is the spatial genetic structuration of four common species of figs within Taiwan? In this part, we will test the hypothesis that even in highly dispersive species such as Ficus, insular conditions may result in niche enlargement and facilitate incipient speciation, as evidenced by strong genetic structuring within Ficus species

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