Patterns and Processes of Evolution in Sundaland

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Transcript of Patterns and Processes of Evolution in Sundaland

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Er is nauwelijks een ander deel van onze aarde aan te wijzen, waar de dierenwereld zulk een verscheidenheid vertoont,

als in den Indo-Australischen archipel.

Dr. L.F. de Beaufort, Zoögeographie van den Indischen Archipel (1926)

Writing a book is an adventure. To begin with, it is a toy and an amusement;

then it becomes a mistress, and then it becomes a master, and then a tyrant. The last phase is

that just as you are about to be reconciled to your servitude you kill the monster, and fling him out to the public.

Sir Winston Churchill

Voor K., J. & F.

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Cover design by Kathelijne Balfoort

Kathelijne Balfoort

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List of papers

This thesis is based on the following papers, referred to by their roman nu-merals.

I. Den Tex, R.-J., Roberts, M., Maldonado, J.E., Munoz-Fuentes, V., Thorington, R. and Leonard, J.A. 2011. Biogeography of the Sunda shelf: a multi species comparison. Manuscript

II. Den Tex, R.-J., and Leonard, J.A. 2011. Speciation and extinction in the Tropics: insights from Asian barbets. Manuscript.

III. Den Tex, R.-J., Thorington, R., Maldonado, J.E., and Leonard, J.A. 2010a. Speciation dynamics in the SE Asian tropics: putting a time perspective on the phylogeny and biogeography of Sundaland tree squirrels, Sundasciurus. Molecular Phylogenetics and Evolution 55: 711-720.

IV. Den Tex, R.-J., and Leonard, J.A. 2011. Red and yellow: the phy-logeography of the coppersnith barbet (Aves: Megalaima hae-macephala). Manuscript.

V. Den Tex, R.-J., Maldonado, J.E., Thorington, R., and Leonard, J.A. 2010b. Nuclear copies of mitochondrial genes: another problem for ancient DNA. Genetica 138: 979-984.

Papers number III ( Elsevier) and V ( Springer) are reproduced with permission from the publishers.

This thesis, or the reproduction in it of any of its manuscripts presented, is not intended for permanent scientific record in the meaning of the Interna-tional Code of Zoological Nomenclature. Thus, any nomenclatural changes proposed here are not valid nomenclatural acts (ICZN, Fourth Edition, Chap-ter 3, Articles 8.2 and 8.3).

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Contents

Introduction ..................................................................................................... 9Tropical biodiversity .................................................................................. 9Origin of tropical biodiversity .................................................................. 10Biogeography ........................................................................................... 10Sundaland ................................................................................................. 12Samples and the importance of natural history museums ........................ 13Ancient DNA and historic DNA .............................................................. 13Main study organisms .............................................................................. 14

Tree squirrels of the genus Sundasciurus ............................................ 14The Asian barbets (Aves: Megalaimidae) ........................................... 15

Research goals .............................................................................................. 17Specific aims ............................................................................................ 17

Summaries of papers ..................................................................................... 18Paper I: Biogeography of the Sunda shelf: a multi species comparison. . 18Paper II: Speciation and extinction in the Tropics: insights from Asian barbets. ..................................................................................................... 18Paper III: Speciation dynamics in the SE Asian tropics: putting a time perspective on the phylogeny and biogeography of Sundaland tree squirrels, Sundasciurus. ............................................................................ 19Paper IV: Red and yellow: the phylogeography of the coppersnith barbet (Aves: Megalaima haemacephala). ......................................................... 20Paper V: Nuclear copies of mitochondrial genes: another problem for ancient DNA. ............................................................................................ 21

Conclusions and prospects ............................................................................ 22

Svensk sammanfattning ................................................................................ 24

Nederlandse samenvatting ............................................................................ 27

Acknowledgements ....................................................................................... 30

References ..................................................................................................... 32

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Abbreviations

aDNA Ancient DNA bp Base pair(s) DNA Deoxy-ribo-nucleic acid LTT plot Lineage through time plot ML Maximum likelihood MP Maximum parsimony mtDNA Mitochondrial DNA MY Million years MYA Million years ago NUMT Nuclear insert of mtDNA origin PCR Polymerase chain reaction SE Asia Southeast Asia

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Introduction

Tropical biodiversity The bewildering array of different life forms, called biodiversity, is not equally distributed over the earth’s surface. Areas of high species richness and high levels of species endemism, that is species that are occurring only in a particular area, are especially found around the earth’s equator (Myers et al. 2000). These areas have a tropical climate and are mainly located in South America, Africa and SE Asia each with particular properties that have shaped the patterns of their own unique biodiversity.

The tropical region of SE Asia is fundamentally different from the other two regions. Scattered over thousands of islands, both large and small with different grades of isolation to each other and the mainland of SE Asia to-gether with its very dynamic geological history, makes this region especially atractive for biogeographers to study the processes that have shaped the pat-terns of biodiversity in this region (Heaney 1986; Gorog et al. 2004). Due to the rapid economical development of this region, large parts of tropi-cal forest habitat, mainly lowland tropical rain forests, are under the serious danger of destruction (Sodhi et al. 2004). These lowland rainforests are the most biodiverse (Lambert and Collar 2002). Threads to these forests are mainly transformation into palm oil plantations and direct logging but also forest fires related to drought years can destroy huge areas of this vegetation (Curran et al. 2004). The importance of tropical rainforests for human soci-ety as a rich source of all kinds of products and from an aesthetic point can-not be overemphasized (Woodruff 2010). Therefore it is important that we should manage these rich sources in such a way that our use of forest prod-ucts will be sustainable and therefore also available to future generations. With the current rate of human induced transformations and population growth, SE Asia is one of the most threatened and vulnerable regions of the tropics (Sodhi et al. 2004; Woodruff 2010). The need for conservation is urgent but to make decisions about where and what to conserve basic and more fundamental knowledge about its biodiversity is necessary (Whittaker et al. 2005). It is in this light that I present my thesis.

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Origin of tropical biodiversity One of the clearest patterns of earth’s biodiversity is that tropical regions house many more different life forms than temperate regions, the so-called latitudinal gradient (Mittelbach et al. 2007). The huge abundance of biodi-versity in the tropics as compared to higher latitudes demands explanation and several hypotheses have been put forward (Mittelbach et al. 2007). The species present in any place is a result of local speciation and extinction dy-namics, and immigration of species from other places (Heaney 2000; Wiens and Donoghue 2004). The two main hypotheses that have been suggested to explain the high density of species in the tropics are the Pleistocene pump hypothesis and the museum hypothesis. One explains the higher diversity through higher speciation, and the other through lower extinction.

The Pleistocene pump hypothesis postulates that much of the diversity present in the tropics today arose in the Pleistocene, as widespread popula-tions were broken into smaller, isolated populations as the climate fluctu-ated. Some of the populations then diverged in isolation, and when the forest was reconnected they increased their distributions and became sympatric with their sister species, and this happened repeatedly. This hypothesis pre-dicts that many of the species in the tropics have a Pleistocene origin.

The Museum hypothesis on the other hand postulates that gradual species built-up through time is responsible for the high levels of biodiversity. Tropical regions are seen as benign environments where extinction rates are low.

Biogeography Biogeography is the study concerned with explaining the observed patterns in distribution of species both in a spatial (geographic) and temporal (his-tory) framework (Whittaker et al. 2005). A phylogenetic approach, by which one tries to reconstruct the evolutionary relationships among species or populations, is imperative for biogeographical studies. Only then, it can teach us to understand about the relative importance of speciation, extinction and dispersal as main drivers that yielded today’s biogeographical patterns. Scale, both spatial and temporal, is important too in biogeographical studies. On a small scale the ecophysiology of species determine the distribution of species in an area (Wiens and Donoghue 2004) but large-scale patterns of species richness are ultimately determined by ecological processes that are linked to dispersal (Wiens and Donoghue 2004).

Extinction, as one of the three main drivers of species richness patterns of a natural group of organisms, is the least well understood because of lack of fossil information for most groups (Raup 1986). However in the absence of fossil data phylogenetic approaches can be used to study extinction (Purvis

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2008) although with extreme caution (Rabosky 2010). In concert with topo-logical tests (Moore et al. 2004) of the structure of phylogenetic trees, ana-lyses of the temporal pattern of splitting events in the phylogeny based on so-called LTT plots, can be used to test which model of cladogenesis, in-cluding models with extinction, fits the observed cladogenesis pattern the best (Nee 2006; Rabosky 2006; Crisp and Cook 2009).

Insights from biogeographical studies can be especially useful for conser-vation because they can illustrate the risks of extinction based on the general theory of island biogeography (MacArthur and Wilson 1967) and identify areas of particular biological interest (Whittaker et al. 2005).

Figure 1. Map of Sundaland and surroundings. Sundaland is made up of the islands lying on the Sunda shelf (Sumatra, Borneo, Java and smaller nearby islands) and the Malay Peninsula. It is bordered on the East of Borneo and Bali by ‘Wallace’s line’. This line delineates the faunal transition between Sundaland and Wallacea and is indicated by the striped red line. Huxley’s line separates the oceanic islands of the Phillipines with the Sunda shelf. Palawan, that is politically part of the Philippines, is considered to be part of the Sundaland. The Isthmus of Kra forms the bio-geographic boundary between Sundaland and the biodiversity hotspot of the mainland of SE Asia known as Indochina or Indo-Burma (Sodhi et al. 2004). The dark continuous dark line shows the limits of the exposed Sunda shelf when sea levels dropped to a maximum of 120 m below the current sea level. The dotted dark line shows the Sunda shelf limits when sea levels are 40 m below current levels (based on Sathiamurthy and Voris 2006).

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Sundaland Sundaland is one of the biodiversity hotspots located in SE Asia (Myers et al. 2000). It comprises of the landmasses of the Malay Peninsula, Sumatra, Java, Bali and Borneo besides smaller islands that are located between them (Fig. 1). Palawan also is considered to be part of Sundaland (Esselstyn et al. 2010). These landmasses are situated on a continental shelf called the Sunda shelf.

Since the last 5 MY the latitudinal positions of the landmasses are more or less stable but the distribution of land and sea area has changed dramati-cally especially since the last 2.5 MY (Hall 1998). During the last 2.5 MY the landmasses of Sundaland were connected and disconnected from each other and the mainland of SE Asia in a cyclical fashion due to dramatic fluc-tuations in sea levels (Fig. 2).

The extent and actual distribution of lowland tropical rainforests when the Sunda shelf was dry land, is not fully resolved. Pollen research has given rise to the idea of the existence of a ‘savanna’ corridor running along the east coast of the Malay Peninsula to the southeast towards Java (Heaney 1991; Bird et al. 2005). This could have worked as a habitat barrier for tropical lowland rainforest dependent organisms (Lim et al. 2010).

Figure 2. Graph that illustrates the changes in global sea level during the past 5 MY (after Lisiecki and Raymo 2005). These fluctuations coincide with global climatic changes that were also responsible for the glacial cycles as known from more north-ern and southern latitudes. The current sea level is high and the recent lowest points correspond with a low stand of 120 m below current levels. Clearly visible is the gradual increase in the amplitude of sea level changes that started around 2.5 to 3 MYA.

Sundaland is surrounded by other biodiversity hotspots. In the North it bor-ders with the Indo-Burma hotspot. This border is located near the Isthmus of Kra (Hughes et al. 2003; de Bruyn et al. 2005). To the East of Sundaland lies

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Wallacea; the border between them is known as Wallace’s line and runs between Borneo and Sulawesi and Bali and Lombok. The oceanic islands of the Philippines form another hotspot and the faunal divide is indicated by Huxley’s line. The terrestrial fauna of Sundaland is mainly of Asian charac-ter with moderate levels of endemism (Corbett and Hill 1992; MacKinnon and Phillipps 1993).

Samples and the importance of natural history museums Current political situations and/or strict regulations regarding sampling fresh tissue material needed for DNA studies in SE Asia, make it very hard if not near impossible to obtain the desired geographical sampling that is needed for biodiversity studies (Sodhi et al. 2007). Natural history museums do hold such geographical sampling of species in their collections. This material, sometimes collected more than 150 years ago, consists for instance of dried tissue skins of birds and mammals but also skeletons and skulls. In the 1990’s it has been shown that a tiny piece of dried tissue, bone or feather from these museum specimens can be used to obtain DNA sequence data (Ellegren 1991; Mundy et al. 1997).

The majority of tissue samples for this study that were used to obtain the DNA sequence data, was made available through the generous willingness of natural history museums around the world. Biodiversity studies like this one for which complete geographical coverage is necessary would be impossible without relying on the rich collections of natural history museums. Therefore the collection of tissue material in natural history museums, that have been built-up over more than one hundred years, is becoming increasingly more important for biodiversity studies (Christidis and Norman 2003; Edwards et al. 2005).

Ancient DNA and historic DNA The genomic DNA extracted from old museum specimens, referred to as historic or ancient DNA, has different properties than DNA obtained from fresh samples. First, the DNA from old specimens is fragmented into small pieces usually in the range of 200 to 300bp in length (Irestedt et al. 2006) so DNA amplification needs to target small fragments. Secondly the DNA can be damaged i.e. nucleotides can be changed, most commonly due to deami-nation that leads to C to T or G to A substitutions (Sefc et al. 2007). Thirdly the DNA concentration can be very low and therefore increases the risk of contamination. Due to the sensitive nature of the amplification of DNA via PCR this problem should not be underestimated. Also, because only a small

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tissue sample is granted, the amount of sequence data that can be generated via traditional Sanger sequencing is limited.

All in all working with these historic or ancient samples poses extra chal-lenges and it is necessary to authenticate thoroughly the obtained DNA se-quence data (Gilbert et al. 2005).

Main study organisms We selected two different unrelated groups of forest dependent vertebrates of which the alpha diversity was relatively well known thereby lowering the risk of missing many (undiscovered) species. Both groups are thought to have low dispersal ability so only when there are favourable habitat corridors available they can successfully colonize new areas or that colonization events are rare measured on geological timescales.

Figure 3. Sundasciurus lowii (Mount Kinabalu, Sabah, Borneo). This is a smaller taxon that occurs on the Malay Peninsula, Sumatra and Borneo and is part of the subgenus Sundasciurus. © Stepanka Nencova.

Tree squirrels of the genus Sundasciurus This genus of tree squirrels is part of a broader radiation of squirrels, the subfamily Calloscuirinae, that mainly occur and are widespread across the mainland of SE Asia and Sundaland. This subfamily of squirrels forms a natural group (Mercer and Roth 2003) and is very species rich with 64 spe-

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cies divided over 14 genera (Thorington and Reeder 2005). The genera Ex-ilisciurus and Sundasciurus crossed Huxley’s line (into the oceanic islands of the Philippines) and Wallace’s line was also crossed, giving rise to three endemic genera on the island of Sulawesi (Corbett and Hill 1992). The total number of currently recognized species in the genus Sundasciurus is 15 and they occur in Sundaland and on the Southern islands of the Philippines (Thorington and Reeder 2005).

They are diurnal in their behaviour but of their ecology and other basic biological facts of these squirrels hardly anything is known. They seem to eat fruit, seeds and small insects (Payne and Francis 2005). Within the genus there is a marked size difference reflected in their taxonomic treatment in two subgenera namely Aletesciurus (for the larger taxa) and Sundasciurus s.s. (for the smaller taxa) but for the rest they have a rather nondescript brownish colouration (Fig. 3).

Figure 4. Megalaima javensis. One of the endemic species of barbet from Java. This species occurs up to 1500 m altitude.

The Asian barbets (Aves: Megalaimidae) The Asian barbets are a bird family that is closely related to the African bar-bets, the South American barbets and toucans (Short and Horne 2001, 2002; Moore and Miglia 2009). They form a natural group and the Asian barbets are basal to the African and South American radiations (Moyle 2004; Moore and Miglia 2009). The barbets and toucans have a pan-tropical distribution

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and are sister to the clade that includes the woodpeckers (Picidae) and Hon-eyguides (Indicatordae; Short and Horne 2001; Hackett et al. 2008).

Currently there are 30 species of Asian barbets recognized (Short and Horne 2002; Rasmussen and Anderton 2005; Collar 2006; Feinstein et al. 2008). They range in size from 17-18 cm to 32 cm in body length. They excavate their own nest hole mostly in dead and decaying trunks, are strongly territorial and have well-developed and stereotyped songs. With the exception of the Brown barbet (Calorhamphus fuliginosus) all species have vivid feather colouration that is mostly confined to the head region (Fig. 4). Their main food resource is fruit, figs (Ficus) being preferred. Most species are confined to wet forests but some species also occur in more degraded habitat and even in human settlements when enough fruiting trees are avail-able. They do not migrate although some altitudinal movements are noticed in species that occur in the Himalayas (Short and Horne 2001, 2002).

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Research goals

The general aim of the investigations during my doctoral studies was to study the patterns and processes that have shaped current biodiversity pat-terns in tropical forest vertebrates of SE Asia, with a focus on Sundaland.

Specific aims More specifically I have:

Paper I. Evaluated the importance of Pleistocene climatic fluctuations in shaping and generating diversity patterns by comparing the phylogeographical patterns of 26 unrelated forest vertebrate taxa across Sundaland.

Paper II. Investigated the role of extinction in the biodiversity patterns of Asian bar-bets by reconstructing and dating a molecular phylogeny of all recognized Asian species.

Paper III. Tested the Pleistocene pump hypothesis and colonization history of the Phil-ippines by dating a molecular phylogeny of tree squirrels of the genus Sun-dasciurus.

Paper IV. Elucidated the evolutionary history of the colour polymorphism in the cop-persmith barbet and its distributional history based on two mtDNA markers and one nuclear marker.

Paper V. Addressed the problem of preferentially amplifying pseudogenes of the mtDNA (NUMT’s) from historical tissue.

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Summaries of papers

Paper I: Biogeography of the Sunda shelf: a multi species comparison. The idea that climatic fluctuations and associated sea level changes during the last 2.5 MY have had large impact on the current distribution of taxa is well established. How this has affected tropical SE Asian forest dependent taxa is much less well known. This is mainly due to the fact that there is no clear agreement on the extent and abundance of lowland tropical rainforest on the Sunda shelf when this area formed land bridges between the different islands situated on the Sunda shelf. We examined the phylogeographical patterns of 26 forest dependent vertebrates that occur across Sundaland.

We found that in 16 taxa the genetic structure showed a pattern whereby the Bornean population was basal to the populations from Sumatra and the Ma-lay Peninsula. The relationship among the different macaque populations showed a pattern of a deep split between the mainland populations and the island populations. The other taxa showed either no geographical structure or an unresolved structure. The temporal cladogenesis patterns showed that there was substantial variation in the estimated time to the most common ancestor for the different taxa that showed a resolved structure. Extinction of populations and subsequent recolonization could explain both these observed topological and temporal patterns. We conclude that the current configura-tion of land and sea creates a situation in which the forest dependent taxa are in a refugial stadium. This makes the current fauna that is dependent on these lowland tropical rainforests extra vulnerable to local extinction when also human mediated habitat loss will further reduce available rain forest habitat.

Paper II: Speciation and extinction in the Tropics: insights from Asian barbets. The tropics are house to a disproportionally amount of biodiversity. In order to understand how, where and when this diversity arose reconstructing (mo-lecular) phylogenies of natural groups of organisms is essential, preferable

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with age estimations of the nodes. We reconstructed a molecular phylogeny of all recognized Asian barbet species (n = 30) and included also multiple (island) populations of the more wide spread species. The dating of the nodes was performed on the mtDNA sequence data and used different cali-bration points from closely related South American toucans and higher taxo-nomic level (family) age estimates based on fossils.

Irrespective of the method used (MP, ML or Bayesian) we recovered a well-supported phylogenetic tree and found that the smaller body sized taxa were basal to a larger group that included all medium to large sized taxa. When analysing the temporal diversification patterns of the Asian barbets the best model that fitted the temporal diversification pattern was a rate con-stant model with high inferred extinction rates; a so-called birth death model. Because such a temporal pattern can also be caused by a clade specific rate increase, we performed a topological tree test that indicated that along a single branch leading to barbet taxa that are mainly distributed across the mainland of SE Asia indeed such a rate increase seemed to have occurred. The clade containing mainly SE Asian taxa fitted a pure birth model whereas the clade containing mainly the Sundaland taxa fitted still a birth death model of cladogenesis. It seems that the current barbet radiation in Sun-daland is significantly shaped by extinction, whereas the radiation composed of mainly mainland taxa evolved under a constant rate model without or with a very low rate of extinction.

We did not find support for the Pleistocene speciation pump hypothesis because no significant diversification rate increase for the whole barbet ra-diation was recovered at around 2.5 to 3 MYA. Because we found some rather high genetic differences among populations of several species that were also morphological rather distinct, we propose several taxonomic changes to better reflect the Asian barbet radiation.

Paper III: Speciation dynamics in the SE Asian tropics: putting a time perspective on the phylogeny and biogeography of Sundaland tree squirrels, Sundasciurus. The tropical region known as Sundaland, the region located on a continental shelf known as the Sunda shelf in tropical SE Asia, is bordered in the north by the Istmus of Kra and by the faunal divides known as Wallace’s line in the east and Huxley’s line in the northeast. This region experienced radical shifts in sea-land distribution during the last 2.5 MY whereby the larger is-lands (Borneo, Sumatra, Java and Bali) on the shelf were repeatedly con-nected and disconnected to each other and to the mainland of SE Asia. This dynamic situation whereby the populations of the different islands were on and off isolated from each other led to the idea that this process could be

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very conductive in generating a lot of diversity and even lead to even speci-ation. To test this Pleistocene speciation pump hypothesis we reconstructed a molecular phylogeny of the tree squirrels of the genus Sundasciurus and dated the nodes of this phylogeny with several different methods and calibra-tion points.

We found that most speciation events occurred well before the onset of the increase of climatic fluctuations around 2.5 MYA. The colonization of the Philippines was estimated to have happened at the beginning of the Plio-cene and probably involved two independent events; first from Borneo into Palawan and then again from Borneo into Mindanao. Unexpectedly we found very deep cryptic divergences among mountain populations on Suma-tra and the Malay Peninsula.

Paper IV: Red and yellow: the phylogeography of the coppersnith barbet (Aves: Megalaima haemacephala). Colouration in birds is important in intra- and inter-specific communication. In this study I investigated the evolutionary history of the two striking colour morphs of the coppersmith barbet. Colour variation within one species can act the starting point for diversification via preferential mating whereby there is preference to mate with one of its own morph. This species is the most widespread barbet species in Asia occurring from Pakistan in the West to the Philippines in the East (were actually it is the only species of barbet). One morph has the supercilium, cheek- and throat patch yellow (the yellow form) and the other morph were the aforementioned patches are red coloured (red form) and the forms are completely allopatric in their distribution. We reconstructed, based on two mtDNA markers and a nuclear marker, the phylogeny of the coppersmith based on individuals sampled over its com-plete distributional range and tested if the populations of each form were more closely related to each other. The red form individuals from Java and Bali were more closely related to the yellow form individuals from Sumatra than to other red form individuals occurring in the Philippines. This pattern of relatedness indicates that the most plausible explanation of the colour change was from yellow to red and that this transformation happened on two independent occasions. From an evolutionary time perspective the colour changes happened very recent and remarkable, happened at nearly the same time in both the Indonesian Archipelago as well as in the Philippine Archi-pelago.

Besides we propose a biogeographical scenario to explain the current phy-logeographical pattern as observed in the coppersmith barbet. Most striking is the absence of this species on the large island of Borneo but it is the only barbet species occurring in the Philippines.

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Paper V: Nuclear copies of mitochondrial genes: another problem for ancient DNA. This paper addressed a more methodological aspect of working with DNA that has been extracted from historic samples. The majority of samples that were used in this study were obtaining from specimens, sometimes more than 150 years old, housed in the collections of natural history museums around the world. Due to the degraded nature of the genomic DNA in these samples short fragments need to be targeted for PCR. Nuclear inserts of mtDNA fragments (NUMT’s) are so-called pseudogenes and can cause seri-ous problems in phylogenetic reconstruction studies if not properly identified as such because these pseudogene sequences are not orthologous. This kind of pseudogenes has been identified in several vertebrate taxa including hu-mans.

We found that when using degenerated primer sets (that is primers that are designed to work across a set of taxonomically related organisms) that targeted short fragments, the probability of preferentially amplifying se-quences that looked like pseudogenes was significantly higher than when using taxon specific primers. Apart from using taxon specific primers an-other method to avoid or lower the risks of amplifying a NUMT is the so-called long range PCR method. Hereby one makes use of the fact that most NUMT’s are short in length by targeting a long stretch of DNA for PCR. This method is unfortunately not feasible in old specimens because of the fragmented nature of the DNA.

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Conclusions and prospects

This study has shown that the dynamic climatic history of Sundaland has left its traces on the current biodiversity patterns of this biodiversity hotspot. We could not find evidence for a rate increase in diversification as stated by the ‘Pleistocene pump’ hypothesis in the Asian barbets. Also most speciation events among the tree squirrels of the genus Sundasciurus predated this geo-logical time frame. This not to say that the climatic perturbations during the last 2.5 MY were not conductive in generating diversity because most of the 17 taxa (out of 27 taxa) that showed phylogeographical structure in Sun-daland were estimated to have been built up during the last 2.5 MY. Mountain populations in Sundaland held unexpected deep cryptic diversity and the finding that within their respective radiations the endemic Bornean mountain barbet species had a basal position shows that the montane fauna of Sundaland is composed of old radiations. This is in contrast with the situation in tropical South America were mountain forms are inferred to be relative young radiations (Weir 2006).

Although working with DNA obtained from old specimens needs to be performed carefully this will be the future for much needed biogeographic studies of this region, because access to fresh tissue samples will be very limited. With the progress in sequence techniques it is foreseen that much more data can be generated from the small tissue samples that natural history museums can provide. The importance of these irreplaceable museum col-lections cannot be overestimated and should be treasured. The last few years we witnessed a remarkable revolution regarding generat-ing genetic data. With the advent of new sequencing techniques this will not be anymore the limiting factor; data authentication and the analysis will be. Together with the developments in phylogenetic reconstruction methods (‘phylogenomics’) and coalescence modelling this will open avenues to test much better the different scenarios that try to identify which processes and their extent have shaped current biodiversity patterns in tropical SE Asia and Sundaland. Preferable more unrelated natural groups of organisms should be included to increase the width of comparative biogeographical studies. With such data sets it will be also possible to test the idea that rates of molecular evolution correlate with latitude.

Our barbet data lends itself to test in a phylogenetic comparative frame-work trade-offs in trait evolution like coloration and song. Besides the cop-

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persmith barbet can serve as a good model in elucidating the possible genetic background in carotenoid coloration and its importance in sexual selection.

Apart from all these more academic questions increased efforts in the con-servation of the biodiversity of this region are even more needed. Given the rapid economic development in SE Asia and therefore the increased pressure on tropical rainforests, it will not be an easy task to prevent further serious degradation and loss of tropical lowland rainforests.

It is my hope that the results of this thesis have contributed to the awareness of how unique this region is and therefore to increase the efforts for protect-ing it from further loss of tropical rainforests. It is our duty to protect and use the riches of these forests in a sustainable way so that future generations can also profit from and enjoy this rich and beautiful biodiversity.

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Svensk sammanfattning

Arters mångfald i tropikerna överväldigar oss om och om igen. Olikheten i livsform, kallad för biologisk mångfald, är resultatet av tre processer som opererar samtidigt, nämligen diversifiering, utdöende och dispersion. För att förstå hur (de tre ovanstående processerna), var (geografisk) och när (tempo-rär) den här biologiska mångfalden har uppstått, bör vi ägna oss åt en histo-risk studie av den ömsesidiga släktskapen mellan organismerna som finns i de här regionerna. Det är dock oklart för flera grupper av organismer hur många sorter det finns överhuvudtaget. Dessutom är vår kunskap för många av sorterna baserad på enstaka eller på sin höjd några samlade exemplar och i de flesta fall fattas grundläggande biologisk information helt och hållet. Därför måste vi nödvändigtvis koncentrera oss på de taxonomiskt välkända grupper som fåglar och däggdjur.

Av de tre stora tropiska regionerna på jordklotet (Sydamerika, Afrika och Sydostasien) utmärker sig Sydostasien, därför att den, i motsatsen till de andra regionerna, består av både en del av Asiens fastland och ett flertal öar av olika storlek. Öarna skiljer sig i isoleringsgrad i förhållande till varandra och Asiens fastland.

Områdets geologiska historia kan kallas dynamisk. Bergformning, plat-tektonik, i samband därmed vulkanism och jordbävningar har format ett amalgam av öar med var sitt ursprung och sin geologiska historia. Någonting som man inte har sett make till i tropikerna.

Klimatologiska på varandra följande förändringar, framförallt i de senaste 2,5 miljon åren, och de därmed förbundna fluktuationerna i den världsomfat-tande havsnivån, var orsaken till en dynamisk fördelning av land och hav. De nuvarande öarna Sumatra, Java, Bali, Borneo och Palawan samt den ma-laysiska halvön kallas för Sundaland och befinner sig på det grunda ”Sunda shelf”. Därför har de omväxlande varit både sammanfogade, genom landbro-ar, och skilda från varandra.

Förutom ett mer akademiskt intresse, finns det också en direkt nytta att bättre förstå uppkomsten av den tropiska biologiska mångfalden, nämligen ur syn-punkten att bevara mångfalden. Just i Sydostasien är den ekonomiska ut-vecklingen snabb och befolkningstillväxten ligger över genomsnittet i värl-den. Därför har trycket på den naturliga hemvisten av olika arter ökat kraf-tigt. Hastigheten i förändringen av den tropiska regnskogen har långtgående

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negativa konsekvenser för överlevnadschanserna för den här unika miljön. Grundläggande kunskaper är nödvändiga för en bra politik i skyddsfrågan.

I den här undersökningen har jag huvudsakligen studerat diversifierings-mönster i två grupper av tropiska vertebrater som inte är nära relaterade med varandra. Vertebrater som till största delen förekommer i och är beroende av den tropiska regnskogen:

Den första gruppen består av trädekorre från slakten Sundasciurus. Deras spridning är begränsad till Sundaland och de södra öarna av den filippinska arkipelagen.

Den andra gruppen är fågelfamiljen av Asiatiska barbetter (Megalaimi-dae). Deras spridning går från Pakistan i väst till Filippinerna i öst, med tyngdpunkten av artrikedom på fastlandet av Sydostasien och i Sundaland.

Deras diversifieringsmönster har jag analyserat genom att rekonstruera deras släkthistoria, eller också deras fylogenetik, med hjälp av användningen av DNAsekvenser av de olika sorterna.

Min jämförande studie baserad på 26 olika taxa, alla beroende på den tropis-ka skogen, visade i 16 fall att populationerna på Borneo skilde sig genetisk starkt från populationerna på Sumatra och den malaysiska halvön. De reste-rande sorterna visade antigen ingen struktur eller en icke-geografisk struktur. Det kan tyda på att de olika populationerna inte eller knappt har haft kontakt med varandra på grund av en komplex förbindelse av hemvisten vid lågt vattenstånd. Det kan också vara så att de olika sorterna har reagerat annor-lunda på de klimatologiska fluktueringarna. Skogsfaunan befinner sig i ett refuginalt stadium och är därmed ännu mer sårbar.

För att testa om de klimatologiska fluktueringarna, och i samband därmed förändringarna i havsnivån, under de senaste 2,5 miljon åren har haft en sig-nifikant påverkan på diversifieringshastigheten, den så kallade Pleistocene pump hypotes, har jag tittat på temporära mönster av diversifiering av träd-ekorre och barbetter. För varken trädekorren eller barbetterna verkade det vara så. De flesta artbildningsmoment av trädekorre uppskattades vara mycket äldre. Iögonfallande var upptäckten av den stora genetiska skillnaden mellan bergspopulationerna på Sumatra och på den malaysiska halvön. Högst sannolikt gick kolonisationen av Filippinerna via två oberoende inva-sioner från Borneo. Av den totala gruppen av undersökta barbetter framgick att en modell med både en konstant diversifieringshastighet och en relativt hög utdöendehastighet passade bäst på det temporära diversifieringsmönst-ret. Den bäst passande modellen till diversifieringen på fastlandet visade sig dock vara en konstant diversifieringsmodell utan hög utdöendehastighet, medan för diversifieringen av barbetterna i Sundaland ännu en hög utdöen-dehastighet implicerades. Några taxonomiska förändringar föreslås.

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I fjärde artikeln har jag studerat den evolutionära historien av de två iögon-fallande färgsammansättningarna hos den vittspridda Kopparslagarbarbetten. Färgvariationen inom en art kan ses som en startpunkt för diversifiering, genom prioriterande parbildning mellan individer med olika färgsamman-sättning, och slutligen resultera i varierande arter. En av de två undersökta Kopparslagarbarbetterna har en tydlig gul färg på kind, ögonbryn och hals (den gula formen), medan hos den andra ovanstående fjäderpartierna är röd-färgade (den röda formen). De rödfärgade från Java och Bali visade sig vara närmare relaterade till de gulfärgade från Sumatra än till de rödfärgade som förekommer i den filippinska arkipelagen. Det här mönstret av släktskap anvisar att den mest sannolika färgändringen har skett från gult till rött och att den här transformeringen har hänt två gånger, oberoende av varandra. Från en evolutionär synpunkt är det en mycket sen färgförändring, som på-fallande nog nästan samtidigt uppträdde i både den Indonesiska arkipelagen och den Filippinska arkipelagen.

Den sista artikeln har en mer metodologisk läggning. De flesta av proverna kommer från naturhistoriska museer, eftersom det numera nästan är omöjligt att samla färska prover med den önskade geografiska spridningen. DNA från de proverna (historisk DNA, ofta kallad för ”ancient DNA”) är mycket fragmenterad och mestadels skadad och befintlig i låga koncentrationer. Oväntad var flerfaldigt förekommande prioriterande amplifikationer av nuk-leära DNAfragment med högst sannolikt mitokondriellt ursprung. Denna information är viktig därför att det finns en risk att icke-orthologa DNA-fragment jämförs med varandra. Användning av universella primers för att erhålla DNAsekvenser av mitokondriellt ursprung bör ske med försiktighet på grund av den förhöjda risken att amplifiera nukleära pseudogener.

Mitt hopp är att mina studier kommer att bidra till en större förståelse för den unika och ömtåliga tropiska biologiska mångfalden i Sydostasien och till en insikt i nödvändigheten av skyddsåtgärder. Dessutom vill jag peka på vikten av att bevara samlingarna vid de naturhistoriska museerna. I framtiden blir det allt svårare att samla biologiskt material från den här regionen. För studi-er om biologisk mångfald (genetisk eller icke-genetisk) är de här samlingar-na av oskattbar betydelse.

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Nederlandse samenvatting

De soortenrijkdom in de tropen overweldigt ons iedere keer. Deze diversiteit aan levensvormen, ook wel biodiversiteit genaamd, is uiteindelijk het resul-taat van drie processen die tegelijkertijd opereren, namelijk diversificatie (soortsvorming), extinctie en dispersie. Als we dus willen begrijpen hoe (de drie bovengenoemde processen), waar (geografisch) en wanneer (temporeel) deze biodiversiteit is onstaan zullen we ons moeten toeleggen op een his-torische studie van de onderlinge verwandschappen tussen organismen die deze regionen bevolken. Een probleem treedt op dat voor veel groepen van organismen het onduidelijk is hoeveel soorten er uberhaupt zijn. Daarnaast is voor veel soorten onze kennis enkel en alleen gebaseerd op één of hooguit enkele verzamelde exemplaren en in de meeste gevallen ontbreekt basale biologische informatie zelfs geheel. Vandaar dat we ons noodzakelijkerwijs moeten richten tot de beter bekende i.c. taxonomisch welbekende groepen zoals vogels en zoogdieren.

Van de drie grote tropische regionen op aarde (Zuid Amerika, Afrika en Zuidoost-Azië) valt Zuidoost-Azië op doordat het, in tegenstelling tot de andere regionen, bestaat uit een gedeelte dat op het vaste land van Azië ligt alsmede rijk is aan eilanden van verschillende grootte en die verschillende mate van isolatiegraad kennen ten opzichte van elkaar en van het vaste land van Azië.

De geologische historie van het gebied is zeer dynamisch te noemen, waarbij gebertgtevorming, plaattectoniek en daarmee geassocieerd vulkan-isme en aardbevingen een amalgaam van eilanden heeft gevormd van ver-schillende origine en met elk een eigen geologische geschiedenis, die zijn gelijke niet kent in de tropen.

Klimatologische opeenvolgende veranderingen, vooral gedurende de laat-ste 2,5 miljoen jaar, en de daarmee gepaard gaande fluctuaties in het wereldwijde zee niveau, zorgden tevens voor een dynamische verdeling van land en zee. De huidige eilanden Sumatra, Java, Bali, Borneo en Palawan alsmede het Maleise Schiereiland (aangeduid met de naam Sundaland) lig-gen op de ondiepe Sunda ‘shelf’ en zijn daardoor alternerend door middel van landbruggen met elkaar verbonden en van elkaar gescheiden geweest.

Naast een meer academische interesse is er ook een direct belang bij het be-ter begrijpen van het ontstaan van deze tropische biodiversiteit namelijk vanuit een beschermingsoogpunt. Juist in Zuidoost-Azië waar de economische ont-wikkelingen zich razendsnel opvolgen en de populatie aanwas van mensen

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boven het gemiddelde van de gehele aarde ligt, is het niet verbazingwekkend dat de druk op het natuurlijk habitat enorm is toegenomen en de snelheid van de huidige transformatie van het tropisch regenwoud verstrekkende negatieve invloed heeft op de overlevingskansen van dit zeer bijzondere leefmilieu. Om goed beschermingbeleid te voeren is basale kennis noodzakelijk.

In dit onderzoek heb ik hoofdzakelijk gekeken naar diversiteitspatronen in twee niet nauw gerelateerde groepen van vertebraten die grotendeels voorkomen in en afhankelijk zijn van het tropisch regenwoud. De eerste groep bestaat uit boomeekhoorns van het geslacht Sundasciurus. Hun ver-spreiding is beperkt tot Sundaland en de zuidelijke eilanden van de Filippi-jnse archipel. De tweede groep is de vogelfamilie der Aziatische baardvogels (Megalaimidae). Hun verspreiding loopt van Pakistan in het westen tot de Filippijnen in het oosten, met het zwaartepunt van soortenrijkdom op het vaste land van Zuidoost Azië en in Sundaland. Deze diversteitspatronen heb ik geanalyseerd door middel van het reconstrueren van hun verwand-schapshistorie, oftewel hun fylogenie, met gebruikmaking van DNA sequen-ties van de verschillende soorten.

Mijn vergelijkende studie gebaseerd op 26 verschillende op het tropisch bos aangewezen taxa liet zien dat in 16 gevallen de populaties op Borneo ge-netisch sterk verschilden van de populaties voorkomende op Sumatra en het Maleise schiereiland. De resterende soorten lieten ofwel geen opgeloste geografische structuur zien danwel een niet-geografische structuur. Enerzijds kan dit wijzen op een complexe habitat connectie gedurende een laagstand van het zee niveau waarbij de verschillende populaties niet of nauwelijks met elkaar in contact kwamen. Anderzijds kan het zijn dat de verschillende soorten sterk verschillend reageerden op de klimatologische fluctuaties. Op dit moment bevindt de bosfauna zich in een refuginaal stadium en is daar-mee extra kwestbaar.

Om te testen of de klimatologische fluctuaties en de daarmee samengaande veranderingen in zee niveau gedurende de afgelopen 2,5 miljoen jaar een significante invloed hebben gehad op de diversificatie snelheid, de zogenaamde Pleistocene pomp hypothese, heb ik gekeken naar temporele patronen van diversificatie in boomeekhoorns en baardvogels. Voor zowel de boomeekhoorns als voor de baardvogels leek dit niet het geval. De meeste speciatiemomenten voor de boomeekhoorns werden veel ouder geschat. Opvallend was de vondst van sterk van elkaar verschillende bergpopulaties op Sumatra en het Maleise schiereiland. De kolonisatie van de Filippijnen verliep hoogstwaarschijnlijk via twee onafhankelijke invasies vanuit Borneo.

Voor de totale groep van onderzochte baardvogels bleek dat een model met een constante diversificatie snelheid en tevens met een relatief hoge extinctie snelheid, het best paste op het gevonden temporele diversificatie patroon.

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Het best passende model voor de diversificatie op het vaste land was echter een constant diversificatie-model zonder hoge extinctie snelheid, terwijl voor de diversificatie van baardvogels in Sundaland nog steeds een hoge extinctie snelheid werd geïmpliceerd. Enkele taxonomische veranderingen worden voorgesteld.

In artikel IV bestudeer ik de evolutionaire geschiedenis van de twee zeer opvallende kleurvormen van de wijdverspreide Kopersmid baardvogel. Kleurvariatie binnen een soort kan namelijk als startpunt worden gezien van diversificatie door middel van preferente paarvorming tussen de verschil-lende kleurvormen en uiteindelijk resulteren in verschillende soorten. Één van de twee vormen heeft een duidelijke gele wang-, wenkbrauw- en keelk-leur (gele vorm) en bij de andere vorm zijn bovengenoemde veerpartijen rood gekleurd (rode vorm). De roodvormigen van Java en Bali waren nau-wer aan de gele vorm van Sumatra verwand dan aan de rode vormen die voorkomen in de Filippijnse archipel. Dit patroon van verwandschap toont aan dat de meest waarschijnlijke kleurverandering van geel naar rood is ge-weest en dat deze transformatie twee maal onafhankelijk heeft plaatsgevon-den. Evolutionair gezien is het een zeer recente kleurverandering en op-vallend genoeg trad deze verandering vrijwel gelijktijdig op in zowel de Indonesische Archipel als in de Filippijnse Archipel.

Het laatste artikel is meer methodologisch van aard. Het merendeel van de gebruikte monsters heb ik van natuurhistorische musea omdat het tegen-woordig vrijwel onmogelijk is om verse monsters te verzamelen met de ge-wenste geografische spreiding. Het DNA uit deze monsters (historisch DNA, vaak ook ancient DNA genaamd) is sterk gefragmenteerd, meestal beschadigd en in lage concentraties aanwezig. Onverwacht was het veel-vuldig voorkomen van de preferente amplificatie van nucleaire DNA frag-menten van hoogstwaarschijnlijk mitochondriale oorsprong. Wanneer dit niet onderkend wordt bestaat het risico dat men niet-orthologe DNA frag-menten met elkaar gaat vergelijken. Het gebruik van universele primers om DNA sequenties te verkrijgen van mitochondriale oorsprong moet met de nodige voorzichtigheid worden toegepast vanwege het verhoogde risico om nucleaire pseudogenen te amplificeren.

Mijn hoop is dat mijn studies zullen bijdragen tot een beter begrip voor deze unieke en zeer kwestbare tropische biodiversiteit van Zuidoost-Azië en tot het inzicht in de urgentie voor de bescherming hiervan. Daarnaast wil ik graag wijzen op het belang van de collecties van natuurhistorische musea. In de toekomst zal het alleen maar moeilijker worden biologisch materiaal te verzamelen in deze regio. Voor biodiversiteits studies (genetisch of niet-genetisch van aard) om onze noodzakelijke kennis te vergroten, zijn deze collecties van onschatbare waarde.

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Acknowledgements

The route a PhD student takes during his studies is unpredictable and full of adventures; feelings of euphoria and frustration go hand in hand. It is un-thinkable to bring such a project to a successful end without the help of other persons. Here I take the opportunity to mention a few. First and foremost I am grateful to my supervisor Jennifer Leonard. Your unconditional support, continuous help and faith in me until the end were of utmost importance to me. I can only say thank you Jennifer that you have given me the opportunity to let me go my own way and let me free but stood beside me when I most needed it. Thank you very much.

Carles Vilà, my second supervisor, your enthusiasm, quick thinking mind and ability to make other people enthusiastic too, have had a stimulating influence on me. Thank you for all your help and advise during the years. I would like to thank you both for organizing the fantastic group meetings in Doñana; great atmosphere and perfect setting to bring the geographically scattered group together and discuss each other’s work. All senior researchers at the Department of Evolutionary Biology I would like to thank: Hans Ellegren, Anders Götherström, Hanna Johannesson, Mattias Jackobsson, Urban Friberg,Tanja Slotte, Jochen Wolf and Simone Immler. The different subjects that you all tackle are a reflection of the highly dynamic nature of the department and I am glad that I got the opportunity to do my PhD here in these stimulating surroundings. Tack! Thanks also to my collaborators from the Smithsonian Institution in Wash-ington DC. Although we never met in person I gratefully thank Richard Thorington and Jesus Maldonado for their input and help regarding sam-pling squirrels for our studies. I thank cordially René Dekker, Hein van Grouw and Steven van der Mije from the Netherlands Centre for Biodiversity Naturalis, Leiden, the Nether-lands. Without their generous help and permission to sample extensively from the collection kept under their care I could not have performed this study. Steven, thank you for providing quick answers from my side on short terms. Ulf Johansson (Naturhistoriska riksmuseet, Stockholm), Paul Sweet (American Museum of Natural History, New York), Jon Fjeldså (Zoologi-cal Museum, Copenhagen) and Mark Robbins (Kansas University Natural History Museum, Kansas) are thanked for providing important samples.

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My stay in Spain at the Estación Biológica de Doñana in Seville has been a remarkable experience for me not in the least to the fantastic people over there! Alejandro thanks for all your help, insightful comments and good laughs; I learned a lot from you. Alberto; the master of GIS. Without your help I would not have such beautiful distribution maps to publish. Jorge big thanks for your guided tour; we did see the Little Bustards hèhè! Inez, Eva and Claudia also big thanks for showing interest in my studies and for being good company and taking me out for tapas! Pim thank you for taking me out on much needed birdwatching trips and for showing so much interest in my studies; I liked and learned from our discussions! Although I was hardly there last year, how important it is to have good office mates was/is shown by the good company of Kristiina and Carina and for-merly Judith. Thanks for the work- and especially non-work related talks, discussions and good laughs!

The members of the former conservation and genetics group at Uppsala are thanked for stimulating and insightful discussions. Violeta your interest and listening ear was very appreciated in times when I needed it the most. I wish you the best of luck in Seville.

To circumvent the risk that I forget people, I would like to thank all the people at the Department of Evolutionary Biology for showing interest in my studies, discussed problems with me, went with me for Thursday-pancakes/sushi or helped me in any other way. Thank you for your good company. Nederlanders in Uppsala: Hugo, Anneleen en de drie koters en Jurjen, Rianne en de drie jongens: dank voor al het medeleven, jullie goede gezel-schap en gewoon om wie jullie zijn. Ik vraag me af wat papa hier allemaal van had gevonden: gedoe met sijsjes en drijfsijsjes hoogstwaarschijnlijk. Moes toch heb jij samen met papa mij de kans gegeven om mijn eigen weg te kiezen en te laten gaan waarvoor ik erg dankbaar ben. Lieve zus, broers, aanhang en schoonfamilie: ook jullie steun op afstand werd en wordt gevoeld en met liefde opgenomen! Lieve Josephine en Frederieke, mijn twee oogappels: dit is nu de samen-vatting van papa’s werk en ik hoef gelukkig niet meer voor zo’n lange tijd naar Spanje. De volgende keer gaan we met z’n allen!

Voor ‘t laatst bewaard en met een reden: lieve Lijn zonder jouw steun en onvoorwaardelijke opoffering zou dit avontuur nooit hebben plaatsgevon-den, laat staan tot een succesvol einde zijn gebracht. Het ei is gelegd dus nu weer tijd voor Frits en Ankie....

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