After the Sarawak Law: evolutionary biology in Borneo since 1855.In February 1855, while taking a rainy season break from his insect collecting at Rajah James Brooke's bungalow in Santubong, English naturalist Alfred Russel Wallace penned a short paper entitled "On the Law Which Has Regulated the Introduction of New Species." He sent the paper to the Annals and Magazine of Natural History, which published it in September of that same year.
In the ten-page article, Wallace elaborated on the phenomenon that related species are always found in close geographical proximity to each other and that species known as fossils usually have their closest relatives in the same geological layer. Drawing the logical conclusion, he proposed the biological law that "Every species has come into existence coincident both in space and time with a pre-existing closely allied species" (Wallace 1855).
The meaning of this "Sarawak Law," as is has become known, is that a new species appears either by the transmutation transmutation /trans·mu·ta·tion/ (trans?mu-ta´shun)
1. evolutionary change of one species into another.
2. the change of one chemical element into another. of an ancestral species, or by splitting off from an ancestral species (without the latter disappearing). Such a sequence of events clearly is supportive of evolution, not of divine creation. Therefore, the paper is generally considered as one of the key steps towards Darwin and Wallace's joint discovery and publication of the mechanism of evolution by natural selection, three years later (Slotten, 2004).
Yet, it would be a misunderstanding to think that his field work in Borneo was what convinced Wallace of the reality of evolution. The 1855 paper draws on a diversity of evidence, but most of it comes from the literature and from Wallace's travels in the Amazon and in Britain--it could have been written anywhere. Nevertheless, by writing his paper in Sarawak, Wallace firmly placed the cradle of evolutionary biology in Borneo. Moreover, his vast zoological collections from the island have been one of the bases upon which further taxonomic and evolutionary work in Borneo has been founded. Consequently, it is of more than passing interest to investigate how evolutionary studies have progressed in Borneo in the one and a half centuries since.
In this paper, I review the main events in Bornean evolutionary biology over the past 150 years. By necessity, this includes mostly research carried out by overseas researchers. Only very recently have evolutionary studies been based in universities and other research institutions on the island itself. I also make comparisons with the situation in parts of the world that are geographically comparable to Borneo. I conclude that, in spite of its auspicious beginnings and a number of beneficial factors, Borneo has played a relatively minor role in the development of evolutionary biology. However, if a shift in research policies were to take place, this situation could soon change for the better.
Background: Evolutionary Biology Worldwide 1855-2005
To place the developments in Bornean evolutionary biology in perspective, let me begin by sketching the main events in this field on a global scale. Darwin and Wallace (1858) and Darwin (1859, 1871) published the outlines of evolution by natural and sexual selection, which have survived essentially unchanged till the present time. However, a comprehensive research program only began to develop in the 1930s, after the broad acceptance of Mendelian genetics (Dobzhansy 1937), the mathematical development of population genetics Population genetics
The study of both experimental and theoretical consequences of mendelian heredity on the population level, in contradistinction to classical genetics which deals with the offspring of specified parents on the familial level. (Fisher 1930), and the thinking of evolution in terms of populations (Mayr 1942). Later, this body of insights (collectively known as Neodarwinism) was complemented with the logical framework for reconstructing evolutionary trees (Hennig 1950). Before the 1930s, very few studies were undertaken with a distinct evolutionary focus. However, data were amassed in systematics systematics: see classification. and biogeography Biogeography
A synthetic discipline that describes the distributions of living and fossil species of plants and animals across the Earth's surface as consequences of ecological and evolutionary processes. that have formed the foundation for later, evolutionary work. Among the major developments in evolutionary biology in the neodarwinian era, I would like to highlight the following:
(1) Phylogenetics phy·lo·ge·net·ics
The study of phylogeny. . The Hennigian method of phylogenetic phy·lo·ge·net·ic
1. Of or relating to phylogeny or phylogenetics.
2. Relating to or based on evolutionary development or history. reconstruction using parsimony par·si·mo·ny
1. Unusual or excessive frugality; extreme economy or stinginess.
2. Adoption of the simplest assumption in the formulation of a theory or in the interpretation of data, especially in accordance with the rule of (i.e. reconstructing evolutionary trees on the principle that the trees that are most plausible require the least evolutionary changes to explain the distribution of characters among species) paved a way for reconstructing phylogenetic trees on a sound philosophical basis. Initially, morphological characters were used for this, later to be taken over by DNA sequences. The latter, and increased computational power, allowed additional and better algorithms to be developed, such as the so-called maximum-likelihood and Bayesian methods, which are very popular today.
(2) Phylogeography. Building on the experience gained with phylogenetic reconstruction of groups of species, more refined genetic dissection and methods of analysis allowed, in the 1980s, the development of phylogeography (Avise et al. 1987). This field aims to elucidate, in detail, the histories of populations within species, including changes in population size, extinction, and migration.
(3) Experimental studies of reproductive isolation (the inability to interbreed interbreed
to breed between animal or plant species, breeds, families. ), hybridization hybridization /hy·brid·iza·tion/ (hi?brid-i-za´shun)
1. crossbreeding; the act or process of producing hybrids.
2. molecular hybridization
3. , and adaptation. Since the early days of Neodarwinism, laboratory studies with Drosophila Drosophila: see fruit fly.
Any member of about 1,000 species in the dipteran genus Drosophila, commonly known as fruit flies but also called vinegar flies. Some species, particularly D. and other model organisms have played an important role in the understanding of evolutionary processes. Parts of the processes of speciation speciation
Formation of new and distinct species, whereby a single evolutionary line splits into two or more genetically independent ones. One of the fundamental processes of evolution, speciation may occur in many ways. (the origin of new species) and/or adaptation have been replicated in the laboratory. Some of the more important outcomes of these studies are the realization that isolation alone does not drive speciation; that natural populations can quickly adapt to very subtle differences in environment; and that reproductive isolation often evolves as a byproduct of adaptation to different environments (Rice and Hostert 1994).
(4) Empirical studies of adaptation and speciation. Early field biologists tended simply to document species and communities, and their variability. This was followed by a period in which evolutionary research moved more and more to the laboratory environment. However, with the rise of scientific field ecology since the 1960s, studying evolution "in action" has represented an important revival of research on real organisms in their natural environment (Weiner 1995). Field observations and experimentation with groups like freshwater fish, birds, fruit flies, etc., have reinforced the notion of the relevance of adaptation and sexual selection in real populations.
Evolutionary Research in Borneo, 1855-1945
The period before the Second World War, essentially the colonial era, saw many naturalists visiting Borneo. Some of the more illustrious collectors, besides Wallace himself, were Italian botanist Oduardo Beccari, who worked with naturalist Giacomo Doria in Borneo in the 1860s, and zoologist John Whitehead, who explored Mount Kinabalu in the 1880s. While they did not analyze and describe their material themselves (and many did not), the specimens were traded, donated, and sold to collectors and museums throughout Europe and North America, usually eventually resulting in taxonomic notes and revisions. A few typical examples of the resulting fragmented literature from that era are Moser (1906) who described two new valgid beetle species from Sarawak, collected by Prof. Gillet; Gude (1918), who described a new species of Everettia land snail from "Borneo," received from "a natural history dealer as far back as 1904"; and Wallace (1865), who named after his host the new "Ornithoptera Brookeiana" which he discovered in Rajah Brooke's other resort, Peninjau.
However, several less haphazard scientific expeditions were also organized to Borneo (and elsewhere in the Malay Archipelago) during this period. For example, German phylogeneticist and embryologist em·bry·ol·o·gist
A specialist in embryology.
an expert in embryology. Willy Kukenthal led a trip (1893-1894) that collected mostly marine organisms that were to form the basis of the collection of Jena University. The results were comprehensively described in a series of expedition reports (e.g., Kukenthal 1897). Doria and Beccari's mollusci collections from Borneo were published in full and authoritatively by Issel (1874) as Molluschi Borneensi. And Whitehead's zoological collections were described by himself and others in a series of papers on ornithology ornithology
Branch of zoology dealing with the study of birds. Early writings on birds were largely anecdotal (including folklore) or practical (e.g., treatises on falconry and game-bird management). , herpetology, mammalogy mam·mal·o·gy
The branch of zoology that deals with mammals.
[mamma(l) + -logy.]
mam , entomology entomology, study of insects, an arthropod class that comprises about 900,000 known species, representing about three fourths of all the classified animal species. , malacology mal·a·col·o·gy
The branch of zoology that deals with mollusks.
[French malacologie, contraction of malacozoologie, from New Latin Malacoz , and ichthyology ichthyology
the study of fishes. (Whitehead 1893 ).
Yet, although very important from a taxonomic and biogeographic bi·o·ge·og·ra·phy
The study of the geographic distribution of organisms.
bio·ge·og point of view, very few of these and other works from the same period can be considered as directly relevant to evolutionary biology. Only here and there, usually as an aside, are allusions made to evolutionary relationships. Whitehead (1893 ), for example, says of the white-breasted wood-swallow (Artamus leucorhynchus), "This bird is called a Tree-Swallow from its habit of flying about after the manner of swallows, and frequently resting on the branches of dead trees; but I should think that, from its mode of nesting and its eggs, it is much more nearly allied to the Shrikes." DNA-DNA hybridization studies a century later proved him correct (Sibley and Monroe 1990). Mostly, though, authors of taxonomic papers of this era use vague terms such as "allied to," "close to," "intermediate between" and "having affinity with" to indicate species' phylogenetic relationships, without attempting any sort of explicit phylogenetic reconstructions.
Another evolutionary subject that was raised by some early authors is the evolution of mimicry mimicry, in biology, the advantageous resemblance of one species to another, often unrelated, species or to a feature of its own environment. (When the latter results from pigmentation it is classed as protective coloration. and camouflage, so prominent among tropical insects. Like Wallace (1869), Whitehead (1893), while collecting in the Pitas peninsula of North Borneo, speculated on the selective pressures driving the evolution of crypsis in birds and insects (which he illustrates), writing that the "ever-waging war" of predators against prey will make sure that "unless a species has some special habit or peculiar form by which it escapes observation, ... it must soon cease to exist." Although falling short of what today we would consider evolutionary biology research, such observations do point out where the relevant questions lie and may have been important for directing later students to fruitful research subjects.
Evolutionary Research in Borneo, 1945-2005
In the history of biology The history of biology traces the study of the living world from ancient to modern times. Although the concept of biology as a single coherent field arose in the 19th century, the biological sciences emerged from traditions of medicine and natural history reaching back to , the period directly after the Second World War is marked by an increase in work from an explicitly neodarwinistic vantage point. Although classical, descriptive work remained the staple of tropical biologists, studies with a distinct focus on testing evolutionary hypotheses began to appear at this time. Below, I give an overview of some of the more important or prominent studies that have been done in Borneo or on Bornean material over the past 60 years, differentiated into several fields. Although the paleoanthropological pa·le·o·an·thro·pol·o·gy
The study of extinct members of the genus Homo sapiens.
pa work in Niah (Cranbrook 2000) and the recent studies of genetics and linguistics (Gray and Jordan 2000) of the Austronesian peoples give Borneo an important position in the debates on human evolution, I will here refer the reader to Baer's (2005) recent review to cover anthropology, and limit myself to studies of non-human evolution.
(1) Paleontology paleontology (pā'lēəntŏl`əjē) [Gr.,= study of early beings], science of the life of past geologic periods based on fossil remains. . Where paleontological pa·le·on·tol·o·gy
The study of the forms of life existing in prehistoric or geologic times, as represented by the fossils of plants, animals, and other organisms. studies attempt to connect fossil forms from one stratum with those from other strata or with recent forms, they can be considered studies of evolution. Unfortunately, such a series of undisturbed sediment layers with relatively short intervals needed for this is rarely found (see, for a good example, Williamson's 1981 study on African freshwater molluscs), and no examples of this kind from Borneo are known, although some palynological (pollen) and marine diatom diatom (dī`ətŏm', -tōm'), unicellular organism of the kingdom Protista, characterized by a silica shell of often intricate and beautiful sculpturing. Most diatoms exist singly, although some join to form colonies. studies (mostly applied to paleoclimatology paleoclimatology
Scientific study of the extended climatic conditions of past geologic ages. Paleoclimatologists seek to explain climate variations for all parts of the Earth during any given geologic period, beginning with the time of and paleoecology pa·le·o·e·col·o·gy
The branch of ecology that deals with the interaction between ancient organisms and their environment. ) could possibly be interpreted evolutionarily (see also below).
(2) Phylogenetics. With the advent of the phylogenetic method in the 1950s, its increase in popularity in the 1970s and subsequent further development of algorithms for phylogenetic reconstruction when molecular data became available in the 1980s, building evolutionary trees has become a standard extension of systematic work. Where earlier taxonomists would describe species and only allude to their evolutionary relationships haphazardly, modern taxonomic revisions often carry explicit phylogenetic hypotheses.
For the Borneo flora and fauna, some good examples of analyses for entire groups are Tanaka et al. (2001a, 2001b, 2003) and Suka and Tanaka (2005), who used mitochondrial DNA to elucidate the phylogeny of the Borneo honeybees (Borneo has five of the eight known honeybees), and Lam (2004), who used nuclear DNA for analyzing the evolutionary relationships between Bornean species of the ginger genus Boesenbergia. As the Borneo biota biota /bi·o·ta/ (bi-o´tah) all the living organisms of a particular area; the combined flora and fauna of a region.
The flora and fauna of a region. has close affinities with other regions within Sundaland, few comprehensive studies are done on Borneo endemics, as most groups of more or less vagile vag·ile
Characterized by vagility; able to move about or disperse in a given environment: a vagile animal species. organisms are distributed over a wider area. Hence, e.g., there are studies of allozyme-based phylogeny of Sundaland shrews by Ruedi (1996), of the mtDNA-based phylogeny of Southeast-Asian flying lizards by McGuire and Kiew (2001), and of the mtDNA-based taxonomy of Malaysian fruit bats (Ryan et al. 2005), which all include many Bornean taxa taxa: see taxon. as well. Phylogenetic studies that focus on clades that are restricted to Borneo are limited to taxa that are either very recent or have limited dispersal capabilities, or both, such as land snails (Schilthuizen et al. 2005).
Smaller studies, aimed at elucidating the phylogenetic position of particular, enigmatic species have also been published, such as Ahlquist et al.'s (1984) use of DNA-DNA hybridization to discover that two endemic birds, the Borneo Bristlehead (Pityriasis pityriasis /pit·y·ri·a·sis/ (pit?i-ri´ah-sis) any of various skin diseases characterized by the formation of fine, branny scales. gymnocephala) and the Fruithunter (Chlamydochaera jefferyi), are related to Australo-Papuan crows, and to the thrushes, respectively. Another example is the study of Fernando et al. (2003), who used mitochondrial DNA and microsatellites to finally prove that the Borneo "pygmy" elephant population is a distinct taxon taxon (pl. taxa), in biology, a term used to denote any group or rank in the classification of organisms, e.g., class, order, family. , having branched off quite early from the Asian elephant Asian elephant
Elaphus maximus. tree, and not the result of feral domestic animals.
(3) Phylogeography. Perhaps more interesting from a Bornean perspective are studies that resolve evolutionary relationships within (endemic) species, as these may reveal patterns of population history within the island. This level of detail has only really been possible with the advent of DNA sequencing and consequently, studies are few, all very recent, and partly yet unpublished. In fact, just five years ago, Sheldon et al. (2001) wrote on a well-studied group like birds, "we do not have phylogenetic or population genetic data on any group of Bornean birds other than the Little Spiderhunter" (referring to Rahman  for the latter). Since then, progress in this field has been considerable. For example, Moyle et al. (2005) used mitochondrial DNA to study the relationships among populations of the White-crowned Forktail (Enicurus leschenaulti) in Borneo. They found that the montane mon·tane
Of, growing in, or inhabiting mountain areas.
[Latin montnus, from m populations were genetically homogeneous and distinct from the lowland populations. The lowland populations separated into a western and a northern group, with the former having affinities with conspecific con·spe·cif·ic
Of or belonging to the same species.
An organism belonging to the same species as another.
Noun 1. populations from Peninsular Malaysia and Sumatra. Similarly detailed phylogeographic scenarios have been constructed for other birds (Rahman 2001, Goh and Rahman 2005, Gawin and Rahman 2005), mammals (Zhi et al. 1996; Han 2000; Han et al. 2000; Warren et al. 2000, 2001; Abdullah et al. 2001; Abdullah 2003; Goossens et al. 2005), Fungi (Hibbett et al. 1995) and other taxa. Ongoing work of this kind will certainly allow generalizations on the paleoecological processes that have shaped evolution in Borneo species.
(4) Empirical studies of adaptation, speciation, and hybridization. Very few studies have been carried out that aim to study the processes of evolution directly, either by experimental or by empirical means. Schilthuizen et al. (2006) studied the evolution of shell shape in isolated snail populations and found effects of both neutral genetic divergence and adaptation to local predators. And, although primarily ecological in focus, several studies have addressed the evolution of ant-plant (Treseder et al. 1995, Fiala et al. 1999, Feldhaar et al. 2003) and fig-wasp (Harrison 2000) mutualisms in Borneo, as well as the evolution of mast-fruiting as an adaptation to seed-predation (Curran and Leighton 2000, Curran and Webb 2000).
The Relevance of Borneo as a Testing Ground for Evolutionary Biology
Overall, Borneo appears to have (or have had) several characteristics that, in comparison with many regions elsewhere in the tropics tropics, also called tropical zone or torrid zone, all the land and water of the earth situated between the Tropic of Cancer at lat. 23 1-2°N and the Tropic of Capricorn at lat. 23 1-2°S. , would appear to make it an ideal place for tropical evolutionary biologists to work. First of all, it has been politically stable. With the exception of the Second World War (1941-1945) and perhaps the period of the Malaysian-Indonesian "Confrontation" (1962-1966), there have been no political upheavals that could have seriously frustrated scientific work. Second, Borneo is rich in elevational and edaphic e·daph·ic
1. Of or relating to soil, especially as it affects living organisms.
2. Influenced by the soil rather than by the climate. (soil) gradients that produce a patchwork of vegetation types and corresponding changes in fauna. This would make the island extra-attractive for students of adaptation and endemism. Third, Borneo has remained environmentally almost untouched until the mid-1950s, and even today most montane forests still are in good shape. Finally, Sabah, Sarawak, Brunei and Kalimantan have all been under the influence of two colonial powers, Britain and the Netherlands, both of which have academic institutions with active and long-lasting research programs in evolutionary biology. Research stations like the Danum Valley Field Centre in Sabah and Wanariset in Kalimantan continue to operate with academic and financial support from the UK and the Netherlands, respectively.
Consequently, one would expect Borneo to figure prominently in the evolutionary literature. However, somewhat surprisingly, this does not seem to be the case. When we peruse pe·ruse
tr.v. pe·rused, pe·rus·ing, pe·rus·es
To read or examine, typically with great care.
[Middle English perusen, to use up : Latin per-, per- conspicuous milestones in the evolutionary biology literature, we find very little usage of Bornean examples. Darwin's On the Origin of Species mentions Borneo only once (in Chapter 11, on representatives of otherwise Australian plant taxa endemic to Borneo's mountains). Reference to Bornean organisms is completely absent from Dobzhansky's (1937) Genetics and the Origin of Species, Mayr's (1963)Animal Species and Evolution, and Coyne and Orr's (2004) Speciation. Ridley's (1997) selection of classic texts on evolution contains several studies of tropical organisms, but none are from Borneo (instead, papers on Hawaiian Drosophila, Amazonian birds, and Galapagos finches are highlighted). And even when one eschews these standard textbooks, studies that first come to mind when one thinks of influential tropical evolutionary biology are, for example, the work on African cichlids (e.g., Meyer 1993, Schliewen et al. 1994, Seehausen and Schuter 2004), and the above-mentioned work on Galapagos finches. My personal collection of journal reprints (about 4,000 entries), which is of course biased towards Southeast Asian work, contains less than ten Borneo-based papers on evolutionary biology. It does, however, contain large numbers of Borneo-based work in forest ecology.
This suggests that, in spite of the work reviewed above, Borneo has not played an important role in the development of tropical evolutionary biology. One can think of several reasons why this may have been so. First of all, Borneo is quite far removed from all important centers of evolutionary biology. At least until about 25 years ago, when air travel became more easily available, this may have discouraged researchers from working here. North American North American
named after North America.
North American blastomycosis
see North American blastomycosis.
North American cattle tick
see boophilusannulatus. evolutionary biologists have tended to work in Central and South America. European ones may have preferred Africa, whereas Australian evolutionary biologists have mostly focused on tropical Queensland. Japan has only recently developed centers for evolutionary biology, and indeed this may increase the amount of Japanese scientists working in Borneo. A second reason may be that Borneo is part of Sundaland, and has been connected with Sumatra, Java and Peninsular Malaysia for much of its geological past. Consequently, it has low levels of endemism. Since endemism has been a feature that has attracted tropical biologists to such areas as Lake Victoria, Madagascar and the Pacific islands, this may be an additional reason why Borneo has been neglected.
On-line bibliographic data bases allow a more quantitive Quan´ti`tive
a. 1. Estimable according to quantity; quantitative. analysis of the impact of Bornean work in evolutionary biology. At the time of writing, the Institute for Scientific Information's Web of Science contained 22.7 million scientific papers from the period 1980-2005. I searched these literature databases using the Boolean search string "(Borneo OR Kalimantan OR Sabah OR Sarawak OR Brunei) AND Evol*." I then excluded all papers on non-organic (i.e. social or tectonic) "evolution." The result was a total of 78 papers. The database also provides the number of times each paper was cited elsewhere, and this allowed me to calculate an average "impact" of 8.7 citations per title. To place these numbers in perspective, I repeated the same procedure for three other geographical regions in the humid tropics, with size roughly equal to Borneo, i.e. Venezuela, Cameroon, and Sumatra. The results are summarized in Table 1.
The results show an interesting pattern. As expected from the general observations above, Borneo scores low on total number of papers, which have on average a moderate impact. The results for Sumatra are very similar, suggesting that it is a consequence of regional biases. In contrast, Venezuela and Cameroon both generate more papers, but their impact is either much higher (Cameroon) or much lower (Venezuela). Although the survey in Table 1 is nowhere near a proper evaluation of the literature, I feel that it is warranted to state that the progress of evolutionary biology in Borneo has been somewhat disappointing and full use of the potential of the island has not been made. Below, I will provide some thoughts on how this situation might be improved in the near future.
Closer inspection of the data upon which Table 1 is based reveals an interesting pattern. Of the four regions compared, the one with the highest number of papers is Venezuela. Among these papers, a relatively large fraction was produced within the country itself. For Borneo, this is not the case: the vast majority of papers were written by foreign (mostly European, American and Japanese) researchers, though sometimes with local co-authors. This suggests that productivity might be increased if more work is carried out fully (that is, field work, laboratory work, data analysis and manuscript preparation, rather than just the former activity) in Borneo itself. Opportunities for this, hardly available previously, have been put in place over the past decade. Several modern universities with state-of-the-art facilities have been built in, for example, Brunei, Sabah, and Sarawak. In fact, many of the papers on DNA-phylogeography in vertebrates reviewed above were conceived and carried out solely by local researchers from Universiti Malaysia Sarawak Universiti Malaysia Sarawak (UNIMAS) was officially incorporated on 24 December 1992. UNIMAS is the eighth University, established just after the declaration of Vision 2020. , a situation that is unique in the history of evolutionary biology in Borneo. In the future, more and more work may originate from local research institutions, rather than foreign ones.
There may be a second reason for this. The regulations put in place under the Convention for International Trade in Endangered Species endangered species, any plant or animal species whose ability to survive and reproduce has been jeopardized by human activities. In 1999 the U.S. government, in accordance with the U.S. (CITES) as well as the national biodiversity legislations (e.g., the Sarawak and Sabah Biodiversity Enactments) prevent indiscriminate collecting and exporting of biological specimens by overseas scientists. Though these legislations are often rightly considered too restrictive and hampering research, they may have as a positive side-effect that overseas researchers will more and more do their laboratory work in research institutions in Borneo itself, reinforcing collaborations with local evolutionary biologists.
Another way for enhancing evolutionary biology would be to make better use of valuable but underused research systems. Mount Kinabalu, for example, is an evolutionary biologist's paradise, with large numbers of well-described endemic species that have adapted along elevational and edaphic gradients. Yet until today, virtually no students of speciation and adaptation have capitalized on this rich biogeographic and taxonomic knowledge base. Other underexploited systems are cave and shallow marine deposits, often already studied by geologists, that presumably pre·sum·a·ble
That can be presumed or taken for granted; reasonable as a supposition: presumable causes of the disaster. contain the undisturbed layers of sediments well-suited for time-series studies of evolutionary change in e.g., land snails and diatoms diatoms
a series of unicellular algae, microscopic in size, with cell walls containing silica. Members of the family Diatomaceae. Their remains accumulate as geological deposits and are mined. See diatomaceous earth. , respectively.
Consequently, the future for evolutionary research in Borneo looks promising. However, it will partly depend on socio-political developments in the countries of Malaysia, Brunei and Indonesia. As mentioned above, biodiversity legislation, if not conceived and enforced appropriately, will hinder, rather than regulate, much valuable research (see also Ng 2000). Another cause for concern is the rapid rise of Islamic creationism, an offshoot of Christian creationism creationism or creation science, belief in the biblical account of the creation of the world as described in Genesis, a characteristic especially of fundamentalist Protestantism (see fundamentalism). , which may tend to make universities wary of installing professorships and research programs in evolution.
Abdullah, M. T. 2003 Biogeography and Variation of Cynopterus brachyotis in Southeast Asia. Ph.D. Dissertation, University of Queensland The University of Queensland (UQ) is the longest-established university in the state of Queensland, Australia, a member of Australia's Group of Eight, and the Sandstone Universities. It is also a founding member of the international Universitas 21 organisation. , Australia.
Abdullah, M. T., C. Moritz, G. C. Grigg and L. S. Hall 2001 Evidence of Cryptic Species within Cynopterus brachyotis by Using mtDNA Sequence. IN: Z. Yaacob, S. Moo-Tan and S.Yorath, eds., Proceedings of the International Conference on In-Situ and Ex-Situ Biodiversity Conservation in the New Millennium, Kota Kinabalu: Sabah Foundation. Pp. 403-8.
Ahlquist, J. E., F. H. Sheldon and C. G. Sibley 1984 The Relationships of the Bornean Bristlehead (Pityriasis gymnocephala) and the Black-collared Thrush (Chlamydochaera jefferyi). Journal fur Onithologie 125:129-40.
Avise, J. C., J. Arnold, R. M. Ball, E. Bermingham, T. Lamb, J. E. Neigel, C. A. Reeb and N. C. Saunders 1987 Intraspecific in·tra·spe·cif·ic also in·tra·spe·cies
Arising or occurring within a species: intraspecific competition. Phylogeography: The Mitochondrial DNA Bridge between Population Genetics and Systematics. Annual Review of Ecology and Systematics 18:489-522.
Baer, A. 2005 Genes, People, and Borneo History: A Review. Borneo Research Council Occasional Papers 2. Phillips, ME: Borneo Research Council.
Coyne, J. A. and H. A. Orr 2004 Speciation. Sunderland: Sinauer.
Cranbrook, Earl of 2000 40,000 Years of Man and Biodiversity in Borneo: An Archaeozoological Perspective. IN: M. Leigh, ed., Borneo 2000: Environment, Conservation, and Land: Proceedings of the Sixth Biennial Borneo Research Conference. Kuching: Universiti Malaysia Sarawak and Sarawak Development Institute. Pp. 1-27.
Curran, L. M. and M. Leighton 2000 Vertebrate Responses to Spatiotemporal spa·ti·o·tem·po·ral
1. Of, relating to, or existing in both space and time.
2. Of or relating to space-time.
[Latin spatium, space + temporal1. Variation in Seed Production of Mast-Fruiting Dipterocarpaceae. Ecological Monographs 70:101-28.
Curran, L. M. and C. O. Webb 2000 Experimental Tests of the Spatiotemporal Scale of Seed Predation in Mast-Fruiting Dipterocarpaceae. Ecological Monographs 70:129-40.
Darwin, C. 1859 On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. London: Murray.
1871 The Descent of Man and Selection in Relation to Sex. London: Murray.
Darwin, C. and A. R. Wallace 1858 On the Tendency of Species to Form Varieties; and on the Perpetuation of Varieties and Species by Natural Means of Selection. Journal of the Proceedings of the Linnean Society, Zoology 3:45-62.
Dobzhansky, T. 1937 Genetics and the Origin of Species. New York New York, state, United States
New York, Middle Atlantic state of the United States. It is bordered by Vermont, Massachusetts, Connecticut, and the Atlantic Ocean (E), New Jersey and Pennsylvania (S), Lakes Erie and Ontario and the Canadian province of : Columbia University Press Columbia University Press is an academic press based in New York City and affiliated with Columbia University. It is currently directed by James D. Jordan (2004-present) and publishes titles in the humanities and sciences, including the fields of literary and cultural studies, .
Feldhaar, H., B. Fiala, J. Gadau, M. Mohamed and U. Maschwitz 2003 Molecular Phylogeny of Crematogaster Subgenus subgenus /sub·ge·nus/ (sub´je-nus) a taxonomic category between a genus and a species.
n. pl. sub·gen·e·ra
A taxonomic category ranking between a genus and a species. Decacrema Ants (Hymenoptera : Formicidae) and the Colonization of Macaranga (Euphorbiaceae) Trees. Molecular Phylogenetics and Evolution Molecular Phylogenetics and Evolution is a prominent scientific journal, popular mostly among evolutionary biologists. Its goal is to make a forum to understand evolution and phylogeny. 27:441-52.
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Arising or occurring between species.
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Table 1 Impact of Evolutionary Biological Literature for the Period 1980-2005 in Borneo and Three Humid-Tropical Regions of Comparable Size Region Papers Average Citations Borneo 78 8.7 Venezuela 167 5.3 Cameroon 91 12.0 Sumatra 50 8.6