Biodiversity Research Center, Academia Sinica


Four major research domains in BRC are: (1) Marine Biodiversity and Ecosystems, (2) Terrestrial Biodiversity and Ecosystems, (3) Evolutionary Genetics and Genomics, and (4) Microbial Diversity and Bioinformatics.

1. Marine Biodiversity and Ecosystems

a. Coral reef biodiversity and coral resilience to climate change

Coral reefs occupy only ~1% of the ocean floor, but harbor ~25% of the marine biodiversity. Thus, the evolutionary relationships of corals and the resilience of corals under the effects of global warming are two important issues.

Our study of the molecular phylogeny of scleractinian corals led to a complete revision of the evolutionary history of this group of corals. Analysis of 127 species representing 75 genera and 17 families from two major coral clades using four different gene loci led to a surprising conclusion that 16 of the 17 coral families studied are not monophyletic. This result is important for the conservation of scleractinian corals, which are reef-building corals, because conservation efforts should be based on correct taxonomy and systematics. Several studies are taken to revise the non-monophyletic families by new morphological characteristics and molecular data.

One of the major unknowns in coral biology is the extent to which coral species and communities can acclimatize or adapt to global warming. Symbiont shuffling - a process whereby a coral may change the type of symbiont that it hosts - is a known mechanism by which some coral species may become less temperature-sensitive, but the extent and significance of this phenomenon at the community level has not been studied previously. Also, it is not well understood whether all the corals in a community can adjust to raising seawater temperatures. The corals living in the outlet area of a nuclear power-plant in south Taiwan and in nearby waters provide a unique opportunity to study how a coral may respond to sea surface warming. A comparison of the coral composition today with a study on the same reef 25 years ago revealed a dramatic shift in the coralassemblages.  However, percent coral coverage has not changed substantially at the heat-stressed area, although coral generic dominance did change.  Also, corals that were affected by thermal effluence were associated with either Symbiodinium clade D (heat-resistant) or combination ofclade C (heat-sensitive) and clade D. Our data showed that coral assemblages can acclimatize to moderate long-term increases in seawater temperature, primarily by changing to host heat-resistant Symbiodinium.  The changes, however, occur at the expense of coral genera which cannot change to host a more heat-tolerant Symbiodinium.

b. Biodiversity of intertidal communities in the Indo-west Pacific region

The Indo-west Pacific region contains the highest marine biodiversity on earth, so studying the factors affecting the diversity pattern is crucial in biodiversity and conservation. Intertidal barnacles are frequently used as model species to study factors affecting the biodiversity, biogeography and phylogeography patterns of marine organisms. We studied the pattern of biodiversity and biogeography of intertidal barnacles in the Indo-west Pacific region, including the West Indian Ocean, South China Sea, Japan and Taiwan waters. Our major results include: (1) We clarified the taxonomy confusions of some major intertidal barnacles in the N.W. Pacific waters and identified several new species in Taiwan, Japan and SE Asian waters to expand and update the biodiversity information. In addition, we published two books to describe and report 94 barnacle species in Taiwan, many of which were new records for Taiwan. (2) Our phylogeography studies revealed that the past sea level lowering in the Pleistocene glacial period and the present day oceanographic currents both have significantly affected the population genetics of intertidal barnacles (Tetraclitaand Chthamalus species) in the Indo-Pacific region. We found a sharp genetic break in the Okinawa region, separating the Japan and Taiwan barnacle populations, which are related to the isolation events in Okinawa during the glacial period. (3) Surprisingly, in addition to natural dispersal mechanisms, we found that some barnacles can be carried by migratory birds and invade new areas, a new route of barnacle migration from the African waters to the Baltic Sea in northern Europe.


2. Terrestrial Biodiversity and Ecosystems

a. Metabolic changes of a subtropical lake ecosystem to typhoon disturbances

Subtropical alpine lakes are usually characterized by highly variable environmental perturbations including typhoon-induced rapid flushing, high diel variation in irradiation, and temperature fluctuations, all of which may affect physical and biogeochemical processes and lake metabolism. Because most lake metabolism studies have been from temperate dimictic lakes, metabolism of tropical and subtropical polymictic lakes, especially those subject to severe, episodic events such as typhoons, is poorly understood.

Our study site is at the Yuan Yang Lake (YYL), a subtropical alpine lake in northern Taiwan. Through the collaboration with University of Wisconsin, we have focused on the effect of typhoon disturbances on hydrodynamics, nutrient cycling, phytoplankton structures and COflux at YYL. Our findings suggest that increased annual precipitation and frequency of storm events led to greater epilimnetic interactions with the watershed and hypolimnion. These interactions resulted in elevated epilimetic CO2 concentrations and therefore greater evasion of CO2.

In addition, we paid attention to the fundamental modeling and to how typhoon strength affects the daily dynamics of ecosystem metabolism of a subtropical alpine lake. We identified proximal agents of typhoon disturbance and assessed the resistance to disturbances and resilience (the rate of recovery after a disturbance) of lake metabolism. Gross primary production (GPP), ecosystem respiration (ER), and net ecosystem production were estimated from high-frequency dissolved oxygen and water temperature data provided by an instrumented buoy.

Ecosystem metabolism in YYL has seasonal patterns similar to those of temperate lakes; however, monthly averages of GPP and ER are decreased by 50% and 25%, respectively, during the typhoon season from their peaks in mid-May. Typhoon effects on ecosystem metabolism is likely mediated by the magnitude and duration of typhoon-induced changes in lake mixing, the quantity and quality of dissolved organic carbon, and the biomass of primary producers.

b. Cooperation and social structure in social animals

How ecology influences cooperation and social structure in social animals is an important issue that has received little attention. Using a game-theoretical model and empirical data of Taiwan yuhina, a cooperatively breeding bird species, we showed that yuhinas employ cooperative strategies under unfavorable environmental conditions. This study is the first combined theoretical and empirical study demonstrating that an unfavorable environment can promote cooperation. We also proposed a general theory that can accommodate all forms of cooperative social groups. It argues that group size and stability can be better understood by studying the conflict between all current group members (insiders) and potential joiners (outsiders) over control of group membership. Also, we distinguish between two major categories of group benefits: resource access benefits (deriving from access to critical resources controlled by the group) and socially produced benefits (resulting from social cooperation among group members). The new framework provides a general predictive framework for studying all taxa that form cooperative social groups.


3. Evolutionary Genetics and Genomics

a. Structure and evolution of chloroplast and mitochondrial genomes in plants

We determined and analyzed the complete chloroplast genome (cpDNA) in 15 representative species of the four extant gymnosperm groups (cycads, ginkgo, conifers, and gnetophytes) and the first mitochondrial genome (mtDNA) of a gymnosperm. (1) Our studies provided the basic data of structural diversity and evolution of cpDNA in gymnosperms. We showed that the reduced gnetophyte cpDNAs resulted from deletions of genes and non-coding sequences, leading to cpDNA compactness and accelerated nucleotide substitution rates. Also, we proposed a model for the loss of large IR regions (ca. 25 Kb) in the black pine. The model was later supported by new data from seven non-Pinus genera of Pinaceae. (2) We elucidated the evolutionary relationships among and within the four major gymnosperm groups. Our subfamilial and generic classifications differ from previous studies in terms of the rank of Cedrus, the position of Cathaya, and the number of subfamilies. (3) A comparison of the Cycas mtDNA with other land plant mtDNAs revealed that noncoding sequences in mtDNAs have been drastically expanded during land plant evolution and that seed plant mtDNAs are much less compact than mtDNAs in other plants. The Cycas mtDNA appears to have been exempted from the frequent gene losses observed in angiosperm mtDNAs.

b. Genetics of speciation in Drosophila

We have been using Drosophila as a model organism to study the genetics of speciation. InDrosophila, pheromonal dienes act as species and sex identity. Our study on the fatty acid desaturase F(desatF) gene, which is involved in the biosynthesis of pheromonal dienes, showed that this gene played a major role in the differentiation of pheromonal dienes. Both the functional divergence in substrate selectivity and the expression shift from bisexual to female-specific and then to loss of expression of desatF have contributed to the divergence of pheromonal dienes, leading to species divergence in the Drosophila melanogaster species subgroup.

We experimentally demonstrated the prevalence of incompatible fitness loci between two young sibling species, D. simulans and D. sechellia. Our competition experiments between D. sechelliaintrogressed DNA segments and the genetic background of D. simulans showed that any introgression placed into a foreign genetic background experienced strong fitness costs and was selected out of the host population. Our observation implies that genome-wide divergence in fitness is extensive even at early stages of speciation.

c. Evolution of gene regulation

There has been much interest in the issue of whether cis or trans regulatory changes are more important in the evolution of gene expression. We used the yeast as the model organism because an experimental protocol can be developed to eliminate environmental effects and to partition the remaining effects into cis and trans components. We first used the pyrosequencing technique to obtain data from more than 200 genes to show that between yeast strains trans changes are far more frequent than cis changes and that this is true even in genes subject to a very simple regulation, that is, for genes that are regulated by a single transcription factor (TF). We were then the first to use the Solexa (Illumina) sequencing technique to obtain genome-wide RNA sequencing data to conduct a detailed analysis of gene expression evolution in yeasts. We showed (1) the prevalence of both trans and cis variation within the S. cerevisiae species, though trans variation occurs much more often, (2) trans variation is subjected to stronger purifying selection than cis variation within a species, and (3) cis divergence appears to have undergone positive selection more frequently than trans divergence in between-species comparison (S. cerevisiae vs. S. paradoxus).

Analyzing epigenetic data from yeasts, mammals, and other eukaryotes, we found: (1) The stronger the nucleosome depletion at the NDR (nucleosome depleted region) of a gene, the more stable (less variable) of the expression of the gene. (2) This observation may explain why the expression of a gene is more stable if it has a very short upstream distance because the NDR tends to highly depleted as it is closely flanked by two (-1 and +1) nucleosomes. (The upstream distance is defined as the distance between the TSS of the gene under study and the TSS or TTS of the upstream gene. TSS: transcription start site, and TTS: transcription termination site.) (3) We found that in mammals head-to-tail (H-T) genes with a short upstream distance are ten times less frequent than head-to-head (H-H) genes with a short upstream distance. We proposed two reasons for this observation. First, the 3' UTR of a gene tends to be longer in mammals than in invertebrates and fungi, so that H-T genes tend to have a longer upstream distance. Second, in the H-T arrangement, the NDR of the focal gene is flanked by -1 and +1 nucleosomes, whereas in the H-H arrangement, it is actually flanked by +1 and +1 nucleosomes because the -1 nucleosome is actually the +1 nucleosome of the upstream gene. For this reason the H-H genes tend to have more stable gene expression when the upstream distance is short and thus tend to be better conserved in evolution thanH-T genes. (The +1 nucleosome is most strongly positioned nucleosome in a gene.) Our study explains the advantage of having a short upstream distance, the advantage of the H-H arrangement over the H-T arrangement and the puzzling observation that H-H genes are common even in higher eukaryotes. In another analysis, we found that overlapping chromatin modifications are better conserved between human and mouse than non-overlapping chromatin modifications. We hypothesized that overlapping chromatin modifications facilitate the binding of a TF to that region.


4. Microbial Diversity and Bioinformatics

a. Coral- and Sponge-associated bacterial communities

We were the first team in Taiwan to report studies on coral-associated bacterial communities. Moreover, we were the first team in the world to develop a Next Generation Sequencing (NGS) approach for studying the population dynamics of a coral associated bacterial community, which can reveal the health condition of the coral. Our approach has been used by other researchers.

In addition, we successfully identified the composition of the bacterial consortium in Terpios hoshinota, a sponge that killed a considerable number of stone corals in Green Island and Orchid Island, causing serious concerns of coral researchers, the public, and the government of Taiwan. Moreover, we have corrected the identity of cyanobacterium, massively associated with the sponge and wrongly believed to be another cyanobacterial species for a long time. Importantly, our study of the bacterial community in the sponge provides insights into the relationship between the sponge and the bacterial associates, and useful clues for further investigations into why the sponge can overgrow on the corals and cause high mortality rates.

b. A new approach to analysis of metagenomic data

Metagenomic study provides insights into uncultured microbial communities. However, at present, taxonomic binning tools for metagenomes discard 30-40% of the data due to the stringency of BLAST cut-offs. To save the discarded data, so as to provide a more comprehensive view of the microbial community, we developed a method to analyze the discarded metagenomes by considering the syntenic conservation of adjacent-neighboring genes. With our method, ~21% of singleton reads could be assigned to taxa. Clearly, our method makes a metagenomic study significantly more informative.

c. Bioinformatics Methods

We report several new methods of bioinformatics. (1) Using a pattern recognition technique in computer science, we developed an efficient method for predicting gapped transcription factor binding sites (TFBSs) in yeasts; gapped TFBSs are discontinuous, making them difficult to predict. (2) We developed new methods for predicting regulatory modules or networks in yeasts, by integrating various types of data.

d. Establishment and maintenance of biodiversity databases

BRC continuously assists the National Science Council and the Council of Agriculture to integrate and update the information of Taiwan biodiversity, including the maintenance of websites of Catalogue of Life in Taiwan (TaiBNET, and Taiwan Biodiversity Information Facility (TaiBIF, one of the nodes for GBIF For all the efforts from Taiwanese taxonomists, the online catalogue for Taiwan native species, with a total number of 53,000 currently, has been constructed, and accordingly Taiwan is one of the few countries that have accomplished this work. In addition, the financial supports from TELDAP program allow us to digitize the specimen information for major academic institutions and museums in Taiwan. Over 1.5 million datasets have been integrated and are open to public online. Besides the catalogue, we make efforts to include the species information, including the basic description, geographic distribution, ecological photos, biota, and references. We are frequently invited to present our databases and the know-hows of database construction and operation.