「系統發生樹」，英文 phylogenetic tree，是一個如何翻譯都翻譯不好的專業詞彙。Phylo- 是指「種族」、genetic 是「基因」、「起源」。我姑且用「演化樹」（evolutionary tree）代替之。演化樹的用處，是以樹狀圖表來表達不同生物（或基因、羣體、個體）的演化關係。大家最有印象的演化樹代表，可能是達爾文於 1859 年《物種起源》所繪的「生命之樹」（tree of life）。

尋找物種起源

要尋找物種起源，我們要向自然學家學習，觀察物種的特徵。以下圖的簡化版「脊椎動物」演化為例，只有靈長類動物和鼠及兔類有「乳腺」，因此它們是演化過程上最相近的，在演化樹上屬於「旁枝」。然後，爬行類和恐龍及鳥類均有「羊膜」但無乳腺，因此它們也是旁枝。兩棲類比起兩組均不相近，所以自己獨自一枝。最後，魚類與其他脊椎動物均不同，因此又是自己獨自一枝。

我們現在只知道這些脊椎動物的演化關係，等於知道這棵「演化樹」是如何分枝，但我們仍然未找出這棵演化樹的「根」。我們無從知道哪一種動物最古老、最接近脊椎動物的起源。

我們只要找到一個比起這些脊椎動物更古老、更不像的生物，例如海星這一類非脊椎動物，把它放置於演化樹上，就可以找到脊椎動物的根。在這個例子裡，海星稱為「外群」（outgroup），它被用來為內群（ingroup）定根。於是，我們便推測得出魚類最為古老、最接近脊椎動物的起源。

（圖五） 以海星（無脊椎動物）作為外群，為「脊椎動物」內群定根。魚類最接近「脊椎動物」起源。紅色標示代表共同特徵。

​

尋找新冠病毒起源

觀察病毒比起觀察動物艱難得多，畢竟病毒太相似，大部分特徵都要在極高倍數的顯微鏡下才可看見，我們無法有效地比較它們的演化關係。如果是同一種病毒（例如新冠病毒），它們在顯微鏡下其實也不會有甚麼分別。我們只可以從它們的「基因」入手。

由一月起，科學家便日以繼夜地為每株病毒定序（sequencing），判定它們的基因序列。你可能知道人類有 23 對染色體（遺傳分子），病毒則簡單得多，只有 1 條遺傳分子（DNA 或 RNA）。這條 DNA（或 RNA）是由一串核鹼基（nucleobase）組成，DNA 的核鹼基有四種：A、T、C 及 G（RNA 的核鹼基以 U 取代 T）。

新冠病毒（SARS-CoV-2）的遺傳分子長度約為 30,000 鹼基，這是其中一個樣本（MN908947）序列的首 1000 位：

「ATTAAAGGTTTATACCTTCCCAGGTAACAAACCAACCAACTTTCGATCTCTTGTAGATCTGTTCTCTAAACGAACTTTAAAATCTGTGTGGCTGTCACTCGGCTGCATGCTTAGTGCACTCACGCAGTATAATTAATAACTAATTACTGTCGTTGACAGGACACGAGTAACTCGTCTATCTTCTGCAGGCTGCTTACGGTTTCGTCCGTGTTGCAGCCGATCATCAGCACATCTAGGTTTCGTCCGGGTGTGACCGAAAGGTAAGATGGAGAGCCTTGTCCCTGGTTTCAACGAGAAAACACACGTCCAACTCAGTTTGCCTGTTTTACAGGTTCGCGACGTGCTCGTACGTGGCTTTGGAGACTCCGTGGAGGAGGTCTTATCAGAGGCACGTCAACATCTTAAAGATGGCACTTGTGGCTTAGTAGAAGTTGAAAAAGGCGTTTTGCCTCAACTTGAACAGCCCTATGTGTTCATCAAACGTTCGGATGCTCGAACTGCACCTCATGGTCATGTTATGGTTGAGCTGGTAGCAGAACTCGAAGGCATTCAGTACGGTCGTAGTGGTGAGACACTTGGTGTCCTTGTCCCTCATGTGGGCGAAATACCAGTGGCTTACCGCAAGGTTCTTCTTCGTAAGAACGGTAATAAAGGAGCTGGTGGCCATAGTTACGGCGCCGATCTAAAGTCATTTGACTTAGGCGACGAGCTTGGCACTGATCCTTATGAAGATTTTCAAGAAAACTGGAACACTAAACATAGCAGTGGTGTTACCCGTGAACTCATGCGTGAGCTTAACGGAGGGGCATACACTCGCTATGTCGATAACAACTTCTGTGGCCCTGATGGCTACCCTCTTGAGTGCATTAAAGACCTTCTAGCACGTGCTGGTAAAGCTTCATGCACTTTGTCCGAACAACTGGACTTTATTGACACTAAGAGGGGTGTATACTGCTGCCGTGAACATGAGCATGAAATTGCTTGGTACACGGAACGTTCT…」（尚餘 28,901 位）。

這些基因密碼就如「脊椎動物」的特徵一樣，帶有演化的資訊。以下是簡化了的病毒演化樹例子，病毒 E、F 有著相同的基因序列，因此它們一組；病毒 C、D 有著相同的基因序列，因此它們一組；病毒 C-D 組和 E-F 組相近（在序列第三位一樣是 A），因此 (C—D)—(E—F)：病毒 B 自己一組；病毒 A 自己一組：

同樣地，我們仍未找到這棵演化樹的根，未能確定新冠病毒的起源。你可能會問，可以找一種與新冠病毒相近的病毒來作為「外群」定根嗎？

現在已知最接近的病毒為以中菊頭蝠（Rhinolophus affinis）作宿主的冠狀病毒 RaTG13（基因序列相似度為 96.3%）。如果我們粗略按照比例來繪畫這棵演化樹，分枝越長代表越多基因變異的話，演化樹會變成這個樣子：

…… 好像有點奇怪。

事實上，當長枝發生於外群時（亦即外群與內群太不相似），外群的演化距離與內群的演化距離太不合比例，內群的基因變異變得不顯著，在運算過程中內群的分枝會出現更多的隨機錯誤，這個現象稱為「長枝吸引效應」（long branch attraction）。這是一個不符合理論的比喻，但最「人性化」容易理解：如果我請你把一堆蘋果分類好，你會認真的看牌子、看標籤；但如果我請你把一堆水果分類的話，你只會想到要把蘋果、香蕉、奇異果等分開，你不會太注意到要把蘋果再細分。

日前劍橋大學發表的論文正正犯了這個錯誤。在這個錯誤下，任何病毒株都有可能錯被放置於上圖病毒 A 的位置，錯被當作最接近病毒起源。
​
造成長枝效應的原因，不外乎是缺少中間的分枝：當中間分枝越多，長枝效應將越弱，外群定根越準確。這些中間分枝是未知的新冠病毒，很有可能寄生在蝙蝠至人類之間未知的中間宿主上，在其中一個中間宿主內，病毒演變至可感染人類。

但無論如何，以我們現今的數據，我們無法用外群來為新冠病毒定根，這是否意味著我們對新冠病毒的起源仍無頭緒？

不，我們還有另外一種尋找物種起源的方法。

​​

新冠病毒的起源和演化路徑

Nextstrain（https://nextstrain.org，附有中文及英文版）是一個實時病毒演化監察平台，搜集了全球科學界所發現的病毒基因序列。Nextstrain 每星期發表研究報告更新現時科學界對新冠病毒的認知，根據美國華盛頓大學流行病學副教授特雷弗．貝德福德（Trevor Bedford）領導發表的最新報告（4月10），團隊共分析了當時已有的 3,160 個基因圖譜，加上分子時鐘（molecular clock），結論出「所有流行中的新冠病毒分株的共同祖先最有可能出現於十一月下旬至十二月上旬的中國武漢。這項發現與中國與亞洲新冠病毒大流行第一個月的情況吻合。」

武漢搜集到的病毒基因變異不多，加上我們已知的其他傳染病學資訊（例如傳播鏈追蹤），科學家認為武漢的病毒樣本最接近演化樹的根，亦即病毒起源。

報告亦提出新冠病毒於全球演化及傳播的路徑：隨著新冠病毒於亞洲爆發，病毒由一至二月開始散播至北美、歐洲及大洋洲，但並未引起大流行及注意，二月至三月於北美及歐洲的病毒開始大量傳播，並於全球大流行，於最近開始傳播回亞洲。

報告（https://nextstrain.org/narratives/ncov/sit-rep/zh/2020-04-10）有最詳盡的演化樹，閱畢《演化樹初探》，你應該可以理解報告中新冠病毒的演化路徑。
​

劍橋大學彼得．福斯特（Peter Forster）所領導的研究團隊日前（4月10日）於《美國國家科學院院報》（PNAS）發表題為《SARS-CoV-2基因圖譜之系統發生網絡分析》的研究論文，重塑新冠病毒（SARS-CoV-2）之早期演化路徑，「有助了解新冠病毒傳播起源」。

研究團隊於全球共享流感數據倡議組織（GISAID）下載 160 個完整新冠病毒基因圖譜，使用系統發生網絡分析（phylogenetic network analysis），分類出三種新冠病毒「變種」，研究團隊將其名為 A、B及C。A株最接近野生動物界的病毒宿主（蝙蝠冠狀病毒 RaTG13），被認為最有可能是新冠病毒起源。原始A株主要發現於武漢病人身上，而 A 株的變種則被發現於居於武漢的美國人、美國及澳洲病人；B 株則遍佈東亞；而 C 株主要散播於歐洲區域，亦見於新加坡、香港及南韓。研究團隊認為：「（這項研究）有助辨別新冠病毒（在不同區域）的源頭，可以對之隔離以阻止病毒進一步散播。」

（圖一） 彼得．福斯特團隊以 160 個新冠病毒基因圖譜重構演化關係，A 株原種於武漢病人身上發現、A 株變種於居於武漢的美國人、美國、澳洲病人身上發現、B 株於東亞廣泛傳播、C 株主要於歐洲。
​

彼得．福斯特團隊的論文引起極大回響，不少媒體甚至錯誤理解論文指出美國有可能為病毒起源，又或者 ABC 三株針對不同人種和群體。隨著時間推進，病毒本來就會因為自然基因變異，演化出不同亞種，但現今科學界仍未發現新冠病毒演化出任何趨勢針對某特定人種。

更重要的是，論文面世僅僅兩日已引起多位流行病學家及基因學家的批評。
 

原始數據已過時

第一，原始論文只於 3 月 4 日分析了 GISAID 當中的 160 個新冠病毒基因圖譜，並未提出論據為何不使用當時已存在的其餘約 100 個基因圖譜。截至今日（4月12日），GISAID 已發表了超過 6,000 個基因圖譜。GISAID 是一個學術界共享數據的平台，科學家透過共同分析數據並發表文章，互相尊重學者對數據的貢獻。這份論文已經不符合現時新冠病毒的最新發展。
 
​
不恰當的假設

第二，原始論文使用了不合適的研究方法和假設，得出無效的結論。GISAID 科學顧問委員會成員、愛丁堡大學分子演化學教授安德魯．蘭博（Andrew Rambaut）批評：「（彼物．福斯特團隊）使用蝙蝠冠狀病毒RaTG13作為外群（outgroup）來判斷新冠病毒起源是錯誤的。」
 
科學界判斷一組物種的起源有幾種方法，其一是使用外群來定根（outgroup-based rooting）。以圖二為例，內群是一組相似的物種，隨時間演進衍生出物種A 至 D，而物種 A 最接近內群的根（共同祖先）。以新冠病毒情況，如果外群與一組 A 區的病毒株相鄰，則可被判斷為 A 區最有可能為病毒起源。

（圖二） 「外群定根法」例子，內群中的 A 最接近外群和內群的根（黃點），因此最有可能是內群中最原始的分支。

​安德魯．蘭博以原始論文所使用的外群（蝙蝠冠狀病毒RaTG13），模擬出外群與所有已知新冠病毒的演化關係（圖三）。

（圖三） ​安德魯．蘭博以彼得．福斯特團隊所使用的外群（蝙蝠冠狀病毒RaTG13），以最大似然估計（maximum likelihood） JC69 模型，模擬新冠病毒與外群的演化關係，紅點為外群。
​

​由圖三可見，蝙蝠冠狀病毒 RaTG13 與其餘所有新冠病毒距離極遠，衍生出長枝吸引效應（long branch attraction），在此效應下，即使兩枝病毒株極不相似，仍會被錯誤歸類相近，而由於所有新冠病毒株互相更為接近，「RaTG13可被置於幾乎任何新冠病毒的鄰枝」，亦即任何地方的新冠病毒株均有可能被錯誤當作起源。因此，研究團隊並不應使用 RaTG13 作外群定根，而應考慮利用分子時鐘模型及其他假設來判斷病毒起源。


論文發表過程成疑

第三，論文的發表過程被質疑。論文其中一位共同作者為考古學家科林·倫福儒（Colin Renfrew），他亦為美國國家科學院的外籍成員。根據《院報》論文發表指引，學院成員有權每年兩次透過「貢獻提呈」（contributed submission）來發表自己的論文，自行選擇論文評審。兩位評審 Toomas Kivisild 以及 Carol Stocking 均並非流行病基因學家，引起其他學者質疑其評審能力。

 
「錯漏百出，令人沮喪」
 
安德魯．蘭博於其推特批評：「（彼物．福斯特團隊的論文）錯漏百出，令人沮喪。他們使用其他學者未公開發表的研究數據（GISAID），以及錯誤的研究假設得出錯誤的結論，竟然被頂尖期刊所接受……（他們）無視了大批學者於基因圖譜上及起源分析上的努力及貢獻。」多位新冠病毒基因專家對此表示同意，並批評《院報》的審稿水準，當中包括英國伯明翰大學微生物基因及生物信息學教授尼克．勒曼（Nick Loman）。


新冠病毒的起源及傳播
 
Nextstrain（https://nextstrain.org）是一個建基於 GISAID 的實時病毒演化監察平台，每星期發表研究報告更新現時科學界對新冠病毒的認知，根據由特雷弗．貝德福德領導於 4月10 日發表的最新報告，分析 3,160 個基因圖譜，加上分子時鐘（molecular clock），結論「所有流行中的新冠病毒分株的共同祖先最有可能出現於十一月下旬至十二月上旬的中國武漢。這項發現與中國與亞洲新冠病毒大流行第一個月的情況吻合。」

報告亦提出新冠病毒於全球演化及傳播的路徑：隨著新冠病毒於亞洲爆發，病毒由一至二月開始散播至北美、歐洲及大洋洲，但並未引起大流行及注意，二月至三月於北美及歐洲的病毒開始大量傳播，並於全球大流行，於最近開始傳播回亞洲。

科學家強烈呼籲大眾要小心應對新冠病毒大流行，應時刻保持社交距離及良好個人衛生，如無必要外出應留在家中，減慢病毒於社區傳播。

（圖四） Nextstrain 團隊最新報告（4月10日），以 3,160 個新冠病毒基因圖譜，加上分子時鐘模型，推斷出新冠病毒演化及傳播路徑，及起源最有可能為十一月下旬至十二月上旬的中國武漢。

資料來源：
​

1. Forster, P., Forster, L., Renfrew, C. & Forster. M. (2020) Phylogenetic network analysis of SARS-CoV-2 genomes. PNAS, 202004999 (early).
2. University of Cambridge. COVID-19: genetic network analysis provides ‘snapshot’ of pandemic origins.
3. Rambaut, A. "There are many things that are terribly wrong about this paper. Both in its content, findings and route to publication." Twitter
4. Bedford, T. et al. (2020) Genomic analysis of COVID-19 spread. Situation report 2020-04-10. Nextstrain.
5. Tang, X. et al. (2020) On the origin and continuing evolution of SARS-CoV-2. National Science Review, nwaa036.
6. Hadfield et al. (2018) Nextstrain: real-time tracking of pathogen evolution. Bioinformatics.

​

With all pleasure and honour, I am appointed to the Meetings Committee of the British Ecological Society for the next three years (2019 - 2022).

https://www.britishecologicalsociety.org/

*********

Founded in 1913 as the oldest ecological society in the world, BES has been promoting and fostering the study of Ecology in its widest sense.

The Society runs several major scientific meetings for ecologists each year. The Annual Meeting currently attracts 1,200 delegates each year and provides the opportunity for ecologists to present papers and posters on a wide variety of topics; an important element has always been the active participation of research students. There is an increasing number of delegates from overseas, principally Europe. It is Europe's largest annual meeting of ecologists. Since 1960 the Society has run an Annual Symposium and published a volume of its papers. It supports a range of other specialist meetings, workshops, training events and field meetings.

(Source: Wikipedia)

I bet you have played Lego before. Have you ever wondered what are the 'Lego blocks' of our life? Many of you may know the answer to it - yes, it is our 'cells'. My newly translated article, 'Building Blocks of Life', unveils the mysteries underlying the cells - giving you a fuller picture how our cells work, and how the diverse forms of life are arisen.

Click here to read the translated article in Chinese
Click here to read the original article in English

This article is published by 'Ask A Biologist', Arizona State University. I am a volunteer contributor of the programme.

​

Evolution is such an amazing process, which gives rises to the current biodiversity. No wonder biologist Theodosius Dobzhansky has said, ‘Nothing in biology makes sense except in the light of evolution.’ My answer to your question is, yes, they are related. And I am going to answer you how this happens in the light of evolution.

From the phylogenetic tree of life, we can see the domain Eukaryota emerges much later than the two other prokaryotic domains. Thus, eukaryotes must have a prokaryote-like ancestor. There are two prominent features that are unique to extant eukaryotes – the presences of (1) nucleus and (2) membrane-bound organelles (mitochondria and chloroplasts are examples). From where do eukaryotes acquire these two things?

When we talk about evolution, we must not neglect the natural environment at the time. Ancient Earth had very little amount of oxygen – of course, the high-energy-making aerobic respiration is not as common as now. There were three types of single-celled prokaryotic organisms: one is a proteobacterium that can make use of oxygen to produce energy (respiration); one is a cyanobacterium that converts light energy to chemical energy (photosynthesis); the last is miserable – it has neither of these abilities. The ‘miserable’ one could be even more miserable – the cyanobacteria were producing oxygen and changing the Earth, but it could not utilize it like the proteobacteria could!

Emergence of First Eukaryote

The ‘miserable’ one now developed infoldings in cell membrane to increase its surface area to volume ratio, possibly because it increased the food intake efficiency to compensate for its lower energy conversion efficiency. The infoldings eventually separated from the cell membrane – forming an endomembrane system, enclosing the nucleoid and genetic materials. This is the first eukaryote (eu, true; karyon, nut; meanings in Greek).

Endosymbiotic Theory (or Symbiogenesis)
 
There came a very rare chance (well, but if you consider how old the Earth is, it is not surprising at all) – The eukaryote engulfed the aerobic proteobacterium, either as food or parasite, scientists are still not quite sure. Both were lucky, the engulfed bacterium avoided the eukaryote’s digestion (Phew!) and the eukaryote assimilated it as its asset to utilize oxygen (Wow!) – no longer miserable! The proteobacterium is now an endosymbiont in the eukaryotic host. This eukaryote is the ancestor of animals, fungi, and other heterotrophs (food-consuming), and the assimilated proteobacteria become the nowadays mitochondria.
 
The increasingly oxygen-rich environment selected away other eukaryotes that had not engulfed the aerobe, because clearly the endosymbiotic eukaryote accumulated energy faster and reproduced faster.
 
At another chance, some eukaryotes took a step further – acquiring the cyanobacteria as endosymbiont. How greedy! But it certainly gained the advantage to produce its own oxygen. This eukaryote is the ancestor of plants, algae, and other autotrophs (food-self-producing), and the assimilated cyanobacteria become the nowadays chloroplasts.
 
Not only does this whole process explain the emergence of eukaryotes, it also explains why we cannot find a cell that possesses chloroplasts but not mitochondria – because proteobacteria won the race!
 
Such transversion from acquisition of endosymbionts (individuals living dependently to each other) to assimilation of organelles (dependent cellular part) is first outlined by Russian botanist Konstantin Mereschkowski, as endosymbiotic theory (or symbiogenesis). Many scientists thereafter advance the theory with more evidence.
 
Evidences of Endosymbiotic Theory
 
Wait a minute! You may say. ‘How do I know this is true?’
 
This endosymbiotic process is estimated to occur around 1.5 billion years ago – it is indeed hard to prove its validity. However, there are still some traces of evidence that are detected by scientists to support this testable hypothesis.
 
First, new mitochondria and chloroplasts have their own genomes not contained in the nuclei – they govern their replication on their own. The cell division process is known as binary fission (many use it and the term ‘amitosis’ interchangeably, but amitosis usually refers to the nucleolar division not involving formation of spindle fibres, and is more frequently referred to certain eukaryotic cells) – which is used solely by prokaryotes.
 
Second, some membrane proteins and lipids are found exclusively in mitochondria, chloroplasts and prokaryotes – including transport protein porins and membrane lipid cardiolipin.
 
Third, genomic comparisons suggest a close phylogenetic relationship between these two organelles and their proposed origins (proteobacteria and cyanobacteria).
 
With more advanced microbiological and genomic studies, endosymbiosis grows from a hypothesis to a sound theory. We are now pretty sure how eukaryotes emerge – but this does not stop scientists from finding solutions of more questions. For instance, biologists utilize mitochondrial DNA to unravel the natural history, and astrobiologists use archaea to find origins of life on Earth and other planets. Scientific inquiry is growing like evolution is.

Douglas R. Holfstadter has made an unprecedented move to bond the mathematician Kurt Gödel, the artist Maurits Corpelis Escher, and the composer Johann Sebastian Bach in the common centre of Gödel’s proof on his incompleteness theorem. This proof is targeting the intrinsic logical looseness and limitations in a formal axiomatic system in mathematics.
 
In a nutshell, mathematicians have been fancying exploiting a list of axioms which could give us “all of the mathematics”: it has to be a complete system – that any given statement is both provable and disprovable; it also has to be a consistent system – that a statement cannot be both proved true and false at the same time. However, such completeness and consistency are inherently contradictory – for example, ‘This statement does not have any proof in the system of Principia Mathematica (PM)’: if this statement is provable, then PM would be inconsistent (PM is self-referentially contradicting); if this statement is unprovable, then PM would be incomplete (the PM lacks the internal proof for it).
 
The mathematical ground of Gödel’s proof itself is a stand-alone masterpiece, but it also steps further to reveal the epistemology of any formal system science – theorems are the branch-outs developed from an axiomatic trunk, extending towards the vast space of truth while some being unreachable, at its counterpart, negative axioms provide the basis of all negations of theorems, also leaving some falsehoods unreachable. Coincidently, this reminds me a Chinese counterpart: Yin Yang Theory, and the symbol itself would give you the intuitive thought of its similarity with Gödel’s proof (Figure 1).

The book is precious in the presentation of such rigorous and complex ideas. First, the dialogue at the beginning of each chapter unveils the limitations that we may come across in our daily lives – such opening encores with the dialogues in Plato’s Symposium. It successfully rings a bell among the readers, preparing the laymen to digest the mathematical and logical paradoxes. Second, the author’s imagination is far beyond mathematics alone: he traces back the connections from Escher and Bach with the Gödel’s theorem, offering a highly vibrant repertoire of aesthetics that is engraved in any field of knowledge. For example, Bach’s canons and fugues are often self-referential to deliver ambiguous perceptions to the listeners. In the meanwhile, many of the Escher’s artwork seem unreal and challenge our intuitive perception of space. Third, at the final portion of the book, it brings out a twenty-first century grand challenge of artificial intelligence, and how it may shed light on resolving the complex systems of self-reference, offering valuable insight to the futurism.
 
This book is definitely a classic that any learners at all stages of knowledge and truth inquiry should read, for the most underlying structure of how we learn and perceive.

Biodiversity loss is one of the top threats in Anthropocene. It is estimated that the current species extinction rate is at 1,000 to 10,000 times the background natural rate (Chivian & Berstein, 2008), because of increasing environmental impacts from anthropogenic activities, including global warming, habitat loss, introduction of exotic species (Thomas et al., 2004). As the extinction of every species potentially leads to the extinction of others in the ecosystem matrix, we may unravel snowballing extinction cascades in the future if proper conservation management is inadequate.

Since last century, many captive breeding programs have been launched to salvage endangered species from imminent extinction (Frankham, 2008). They are vibrant in the highly diversified forms: a university lab, a joint conservation group or a zoo. They have been targeted to serving for a wide range of conservation purposes: (1) the crucial goal in maintaining genetic integrity of threatened species; (2) the pivotal role of translocation and re-introduction programmes that restore wild population (Grueber et al., 2015); (3) educating people of the importance of wildlife conservation; and (4) substantiating in-depth research opportunity for future applications.

Captive management is utterly important when the species can no longer sustain the population itself in the wild. Besides the human activities, natural catastrophes such as strong predation pressure, diseases and food shortage can also endanger wild species to an unsecured population. For example, pink pigeon (Nesoenas mayeri) once experienced a population shock down to 10 individuals, thus is enlisted in IUCN Critically Endangered in 1994. They suffered from introduced invasive species (Swinnerton, 2001) and intense food competition (Jones & Owadally, 1988). The compounding effect of captive breeding and reintroduction have been successful to bring back the survival likelihood. It has been downlisted to Endangered and may become eligible for further downlisting in the future. Captive breeding is beneficial to concentrate the resource and management effort, as compared to in-situ conservation, especially when the population is small and vulnerable to natural chance events. Other successful reintroduction examples include scimitar-horned oryx, Californian condor and golden lion tamarin.

The rationale behind the educational purpose of a captivity such as zoos and marine parks is the created affective connections bridging the nature and visitors. In compared to alienated forms of conservation outreach, such as propaganda and leaflets, the actual experience spending with an animal quickly strengthens the bonding and thus raise a higher compassion to save the endangered animals. When reports find out that there are positive effects of zoos on cognitive and affective characteristics (Luebke et al., 2016), captive management breaks the estrangement between public and wildlife, and affirms the community engagement of conservation.

The success of species conservation depends much on our understanding of their behavioral ecology, habitat and reproductive biology. Captive breeding enables researchers and conservationists to study and experiment the mating success and optimal environmental factors that are most favorable to the species. Especially when certain endangered species is endemic and possesses unique physiology, such as keel-scaled boa in Round Island (Casarea dussumieri) (Bloxam & Tonge, 1986), captive breeding safeguards a better prospecting future of the conservation of the species and its closely related relatives. Further genetic and molecule tools can enable us to minimize inbreeding and maintain the genetic diversity by implementing carefully planned captive management, increasing the chance of successful adaptation to the environment upon reintroduction or translocation (Witzenberger & Hochkirch, 2011).

The three pillars of conservation, education and research in captive management are entwined to conserve the endangered species. However, the effectiveness of captive breeding stirs up some debate as more limitations and inadequacies are untangled.

Captivity may be time consuming but rewarding less, failing to improve the conservation status or mitigating the declining population. For example, the habitat of Hainan gibbons (Nomascus hainanus) is severely fragmented and degraded by infrastructure development (Cawthon Lang, 2005). However, their reproduction biology is sophisticated and discerns great effort. Without a proper mating ground, their lack of territories is a prominent reproductive barrier in the wild (Zhou et al., 2008). Although attempts have been made to breed Hainan gibbons in captivity, all have been failed and the captivity plan is abandoned. Currently there are no Hainan gibbons in captivity (Geissmann, T. & Bleisch, 2008).

Latest findings report that students demonstrate no positive learning outcomes at all (Jensen, 2014). The paper concludes, that zoos fail to nurture proactive conservationists among students and empower the pupils to take ameliorative actions. This research conflicts with the common belief that zoos can function as an important education source. The possible reason behind is the differential management of educational programmes in different places, and the report is locally-targeted. It sheds light on the limitation that different zoos take different approaches in delivering education, while some succeed, some have week efforts.

There are disproportionate efforts allocated to certain species because of an anthropocentric view of conservation effort. A better-known example is the ‘panda-centric conservation’ in which Chinese government has invested tremendous conservation funding for its captive management. Giant panda costs each hosting captivity an average of 2.6 million dollars a year, and the cost can compound to 4 million when cubs are arisen (Warren, 2006). The great financial commitment exerts strong burden to the government, NGO and the public. As a result, ‘flagship species’ is the conservation marketing strategy that attracts public awareness and financial donation. However, it potentially skews the conservation priorities in sole humans’ favour and the detrimental species receive less attention (Ducarme, Luque & Courchamp, 2013). Particularly when the panda is successfully downlisted to Vulnerable in IUCN, the flagship may disappear and poses negative impacts on the attitudes of the conservation stakeholders (Simberloff, 1998).
​
Captive management is undoubtedly an indispensable tool to preserve a ‘insurance population’ for endangered species. However, the daunting crisis of species extinction must be faced squarely and ex-situ conservation is only the last resort to rescue those species in the edge. In-situ conservation, habitat preservation and better wildlife management must be prioritized and captivity is not an excuse to avoid them.

 
References

1. Bloxam, Q. M. C. B. & Tonge, S. J. (1986). The Round Island Boa Casarea dussumieri Breeding Programme at the Jersey Wildlife Preservation Trust. Dodo: Journal of the Jersey Wildlife Preservation Trust, 23, 101–107.
2. Cawthon-Lang, K. A. (2005). Primate Factsheets: Orangutan (Pongo) Behavior.
3. Chivian, E. & Bernstein, A. (eds.) (2008). Sustaining life: How human health depends on biodiversity. Center for Health and the Global Environment. Oxford University Press, New York.
4. Ducarme, F., Luque, G. M. & Courchamp, F. (2013). What are "charismatic species" for conservation biologists? BioSciences Master Reviews, 1.
5. Geissmann, T. & Bleisch, W. (2008). Nomascus hainanus. IUCN Red List of Threatened Species, Version 2013.2. International Union for Conservation of Nature.
6. Grueber, C. E., Hogg, C. J., Ivy, J. A. & Belov, K. (2015). Impacts of early viability selection on management of inbreeding and genetic diversity in conservation. Molecular Ecology, 24(8), 1645–1643.
7. Jensen, E. (2014). Evaluating Children’s Conservation Biology Learning at the Zoo. Conservation Biology, 28(4), 1004–1011.
8. Jones, C. G. & Owadally, A.W. (1988). The life histories and conservation of the Mauritius Kestrel Falco punctatus, Pink Pigeon Columba mayeri and Echo Parakeet Psittacula eques. Proceedings of the Royal Society of Arts and Sciences of Mauritius, 5, 79–130.
9. Luebke, J. F., Watters, J. V., Packer, J., Miller, L. J. & Powell, D. M. (2016). Zoo Visitors' Affective Responses to Observing Animal Behaviors. Vistor Studies, 19(1), 60–76.
10. Simberloff, D. (1998). Flagships, umbrellas, and keystones: Is single-species management passe in the landscape era? Biological Conservation, 83, 247–257.
11. Swinnerton, K. (2001). Ecology and conservation of the Pink Pigeon Columba mayeri on Mauritius. Dodo: Journal of the Jersey Wildlife Preservation Trust, 37, 99.
12. Thomas, C. D., Cameron. A., Green, R. E., Bakkenes, M., Beaumont, L. J., Collingham, Y. C. …Williams, S. E. (2004). Extinction risk from climate change. Nature, 427, 145–148.
13. Warren, L. (2006). Panda, Inc. National Geographic Magazine, July 2006.
14. Witzenberger, K. & Hochkirch, A. (2011). Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodiversity and Conservation, 20(9), 1843–1861.
15. Zhou, J., Wei, F., Li, M., Chan, B. P. L. & Wang, D. (2008). Reproductive characters and mating behaviour of wild Nomascus hainanus. International Journal of Primatology, 29, 1037–1046.