Cockroach vs. human arms race

German cockroach (via Wikimedia Commons)

The cockroach is a creature that universally elicits feelings of disgust, but anyone who has tried to catch or kill them would also concede a grudging admiration for their toughness. They thrive on the refuse of our human civilization, and it has been said that if the human race somehow managed to wipe itself out through nuclear war, it would be cockroaches that flourish in the ruins.

Much human ingenuity has also gone into designing new and improved ways to kill cockroaches. Sugar laced with poison is commonly used to bait and exterminate these pests. The large-scale deployment of such traps, however, also constitutes a huge inadvertent experiment on the effectiveness of natural selection. Some populations of the German cockroach, Blatella germanica, have become immune to such traps because they are no longer attracted by the glucose sugar used as bait.

Recent research by a team from North Carolina State University (article abstract) has uncovered the physiological basis for this glucose aversion. The sense of taste is mediated by gustatory sensory neurons (GRNs); different substances activate different neurons and trigger different behavioral responses. In normal, wild-type cockroaches, glucose stimulates sugar-GRNs. The researchers found that this is also the case in the glucose-averse cockroaches, but that glucose also additionally stimulates bitter-GRNs, which are usually simulated by substances such as caffeine to which cockroaches are averse. The activation of bitter-GRNs suppresses the usual response of sugar-GRNs and causes the glucose-averse behavior.

This is a nice and neat story that illustrates how quickly natural selection can act, especially considering how numerous the cockroaches must actually be. Whereas evolutionary arms races between most organisms are limited by the rate at which natural selection can act, our human battles against the organisms that we consider pests and weeds are accelerated greatly by the pace of technological change and innovation. This episode shows, however, that natural selection can sometimes keep up and catch us when we are not wary.

How periodic cicadas evolved their timing

Every few years, the periodic cicadas come into the news, when they simultaneously complete their life cycles and emerge from the ground as winged adults. They swarm over large parts of the eastern United States and attract both curiosity and alarm from residents and the media. After a few weeks, their mating and egg-laying over, they disappear just as quickly as they appeared. Of course, they are not completely gone: their juveniles live underground, having perhaps the longest maturation of any insect, to emerge as adults after a period of 13 or 17 years.

13-year cicada from Brood XIX. Via Wikimedia Commons.

Why 13 or 17 years? These prime-numbered periods have puzzled more mathematically-minded biologists for ages, with one suggestion being that a prime-numbered life cycle would minimize the number of predator life cycles that could synchronize with it (because a prime number has no factors but itself). But how did this situation evolve?

A new paper published in PNAS (open access) from a group of Japanese scientists looks at the phylogeny and population genetics of the known species of periodic cicadas. The periodic cicadas fall within the genus Magicicada, within which are species partly defined by the length of their period. M. tredecim for example is a 13-year species, while M. septendecim is a 17-year species. Within each species there are also multiple "broods", representing different cohorts have the same emergence and mating cycles. One brood may encompass multiple species. Siva blogged here about one such brood in 2004, the ominously-named Brood X, which had an unusually large emergence (the "X" is actually just a roman numeral). The different species fall within three species groups, each with both 13- and 17-year species.

Contrary to expectations, the old species, defined by morphology and period, do not correspond to the evolutionary history as uncovered by molecular phylogeny and haplotyping. The three big species groups are still supported, representing two evolutionary splits at about 3.9 and 2.5 million years ago (Mya). The splits within the species groups, however, are relatively recent, mostly less than 0.5 Mya. Furthermore, the splits correspond more to geographical regions than to life cycle period. The split between 13- and 17-year periods have also evolved multiple times. To quote from the paper:

Our results are broadly consistent with the previous idea that an ancestor of all Magicicada diverged into three species allopatrically, and later, the three became sympatric and each species independently diverged into 13- and 17-y cicadas. Surprisingly, however, the divergence of 13- and 17-y cicadas was asynchronous among the species groups and occurred repeatedly even within a species group. This finding is all of the more interesting given that each species group shows similar eastern, middle, and western phylogeographic divisions similar to post-Pleistocene patterns observed in other North American taxa, suggesting that the three Magicicacda groups shared multiple refugia during the last glacial maximum.

This is a nice surprise, and as the authors point out, the repeated switching between 13- and 17-year forms suggests that there is a single genetic "switch" involved, because it is unlikely that a complex mechanism could be repeatedly gained and lost in such a manner.

Carl Woese, Discoverer of the Archaea, RIP

One of the first things that students learn today about the diversity of life is the concept of the Three Domains of Bacteria, Archaea, and Eukarya. In the past, they would have learned about the Five Kingdoms — Prokaryotes, Animals, Plants, Fungi, and Protists —a concept popularized by the late Lynn Margulis, but we now know that the animals, plants, and fungi are relative newcomers on the evolutionary scene, and that the "prokaryotes" actually contain two ancient lineages, the Bacteria and Archaea, which split long before the eukaryotic kingdoms.

Carl Woese in 2006, via U Illinois

For this insight, we can thank Carl Woese, who passed away just before the New Year at the age of 84 (U Illinois press release, NY Times obituary). Woese made his discovery in the 1970s, when sequencing DNA and RNA was anything but routine. At that time, the prokaryotes were classified primarily by physiological characteristics and morphological appearance. There was little attention paid to microbial evolution, except in a speculative way, simply because there was no easy way to go about studying it.

Lynn Margulis - an appreciation

Lynn Margulis passed away recently at the age of 73 (NY Times obituary). She was responsible for one of the great ideas of modern biology -- the endosymbiotic theory for the origin of organelles. This is the idea that chloroplasts and mitochondria of eukaryotic cells originated as independent prokaryotes that became associated symbiotically with host cells, and eventually became indispensable organelles. The whole process she called "symbiogenesis". Siva blogged about this here two days ago, and suggested that I share something to.

The story of the theory itself is also quite well known. Margulis put forward the hypothesis in a paper titled "On the origin of mitosing cells" (Journal of Theoretical Biology 14: 225, under her married name L. Sagan - PubMed, ScienceDirect) in 1967, but before it was accepted for publication there, it had been rejected 15 times by other journals. It was initially controversial--to think that an essential part of our own cells are actually bacteria in disguise!--but today it is textbook knowledge. Much like the theory of plate tectonics, this is one of the great Cinderella stories of modern science.

I was fortunate enough to hear Margulis speak a few years ago when I was in college. I don't remember the details now, but I do remember a few things she said. She recalled that the last time she was at Harvard, it was at a seminar where Ernst Mayr (one of the pioneers of the Neo-Darwinian Synthesis) was in the audience, sitting right there; she pointed at the seat in front of my friend Noor and me and we got a little thrill from it. "Although he was almost a hundred years old, he was still the sharpest mind in the room!"

(She wrote a reminiscence of Mayr when he passed away in 2005, which gives some flavor of their personalities. Mayr: "You don't have to tell me what 'symbiosis' is! I studied symbiosis with Paul Buchner in Griefswald [in the 1920s]." Buchner later wrote one of the classic books on symbiosis, Endosymbiose der Tier mit pflanzlichen Mikroorganismen.)

She also showed a video of protists from termite guts, some of which have symbiotic bacteria living on their surface, which act more or less as surrogate flagella. One could tell that she was really captivated by the beauty of these organisms, and I heard later from someone that she often showed this video at her talks.

Margulis's 1967 paper is best known for its hypotheses about chloroplasts and mitochondria, which have been validated by lines of evidence, such as DNA sequencing, that were not available to her at the time. Her remaining hypothesis was that eukaryotic flagella evolved from symbiotic spirochaetes, which are corkscrew-shaped bacteria that swim helically. This idea hasn't done so well, and hasn't been supported by evidence in the way which the chloroplast and mitochondrial hypotheses have, but as her fascination with the video shows, she was still thinking about it. One of her last papers, published in 2010, was on the microscopical structure of one kind of these bacteria on a termite-gut protozoan.

On rereading her 1967 paper, a few things stood out to me. She managed to synthesize a tremendous amount of information (the paper is 49 pages long) from very different fields, including microbiology, palaeontology, geology, cytology, and evolution.

This was where she first put forward many of the concepts and themes which she would continue to think about and work on for long afterwards. For example, the scenario for eukaryote evolution that appears as a figure is re-presented in modified form in her popular book, Five Kingdoms.

The book, which she coauthored with Karlene Schwartz, was one of my favorite books as a student. The latest edition is from 1998, but it's still a good read, giving a brief overview of all the major phyla of living organisms in the classical five kingdoms: Prokaryotes, Protoctists (i.e. protists), Plants, Fungi, and Animals. It was my first introduction to the weird and wonderful world of protist and microbe diversity, which otherwise get such short shrift in introductory biology. It also shows how effective she was as an encyclopedic collator and system-builder.

In her thoroughness she also delved into the older literature. She had an interest in the history of biology, and what might be called her intellectual predecessors. She was involved in a recent project to translate a 1924 Russian book titled Symbiogenesis: A New Principle of Evolution by Boris Kozo-Polyansky. She did not shy from acknowledging these "forbears" and other early insights and ideas that were "before their time".

I think that she represented a very "classical" sort of biology, informed by visual thinking and reasoning by analogy. Looking at older books of zoology, botany, or cytology, one finds a similar frame of mind and emphasis on pattern-recognition. Modern biology is definitely still about pattern-recognition, but much of it is now impossible to "eyeball", such as searching for gene homology.

Unfortunately, reasoning by analogy can sometimes lead us down the wrong track, and an over-enthusiasm for it seems to have been responsible for a controversy that involved her in 2009. As a member of the National Academy of Science in the USA, she sponsored a paper for publication in its Proceedings, which hypothesized that "caterpillars evolved from onychophorans [velvet worms] by hybridogenesis" with insects. The paper never made it into print, but attracted a storm of protest and the imputation that she misused the submission process to push through a paper which would never have been published elsewhere.

That episode didn't help her reputation for "eccentricity", which is a word which seems to crop up in describing her, alongside "maverick" or "rebel". Nonetheless, her place in biology is secured, and I think it's important to acknowledge why. She gave us a whole new way of thinking about evolution, spurred scientific interest in endosymbiosis and early evolution, brought protists and other formerly obscure organisms to the attention of scientists and public, and defended the importance of symbiosis to the evolutionary process.

In doing so, Lynn Margulis gave us a glimpse into the biological world as it could have been at its origin, and also into the present, where we still make regular use of the concepts that she pioneered. RIP.

The world's largest virus

Back in January I blogged about how the physical constraint of capsid size may be forcing some viruses to squeeze their genomes into such a compact state that their genes overlap. Now we visit the other end of the scale to the largest virus yet discovered, appropriately called Megavirus chilensis, found in ocean waters off the coast of Chile.

As one of the paper's coauthors told BBC News, "You don't need an electron microscope to see it; you can see it with an ordinary light microscope." Each virus particle is about 680 nm across, or just under a micrometer, making it just barely visible as specks by light microscopy. They're structurally interesting, bearing a covering of fibers ("hair") all over the surface, and a five-pronged star-shaped structure on one vertex that the authors have called a "stargate", which the virus uses to release its nuclear material into the host cytoplasm.

The agave's big bang

One of the condominiums near my home has a bit of fancy horticulture at the entrance. Lined up along the road is a row of big agave plants, and lately four of them have been at various stages of flowering. If you haven't seen an agave plant (also called "century-plants") flowering, it's a sight to behold: the succulent leaves are thick and waxy, forming a rosette close to the ground, and from the middle emerges a spike-shaped stalked reaching taller than a person, from which the flowers will eventually unfurl.

Agave plants flowering in Portugal (Wikimedia)

The agave plants (see the Agavaceae webpage for more photographs) are also known as century plants because of a misconception that they only flower once a century. It is true however that it can take up to several years or even decades before an individual plant flowers. Once it does so, it apparently withers away and dies. For this reason, probably, in some of the plants that I saw, the flower stalks were cut away soon afterwards.

Why would any organism only flower once in its lifetime? Doesn't natural selection reward those who have more offspring? Isn't having only one crop of offspring akin to putting all your eggs in one basket?

Do chimps have culture?

It's hard being human, or at least, to define what exactly makes us human. It used to be tool-making, but our close cousins the chimpanzees have been found to use tools, such as sticks to gather insects for food. Could culture, the inheritance of behaviors by learning, be the next "exclusively human" trait to fall?

Evolutionary anthropologists are studying chimpanzee communities throughout the West coast of Africa to determine if different groups indeed have different cultures and traditions. There is geographical variation in what specific behaviors chimps exhibit, but this alone does not confirm that there are different traditions:

Deciphering culture in the wild is difficult because researchers must ensure that behavioural differences between groups do not have other causes, such as variation in genetics or environmental conditions. "Why is it all chimps don't do everything? One solution is that there are hidden ecological differences between populations," says primatologist Richard Wrangham at Harvard University in Cambridge, Massachusetts. A behaviour could be linked to any number of variables such as amount of rainfall, the types of tree available, or the kinds of predator in the area, he says.

Read more at Nature News.

The mole's new thumb

Two instances of making do with what you have at hand.

With their huge hands, pointy snouts, and apparent lack of eyes, moles certainly appear to us as very peculiar creatures. These traits, however, are adaptations to a subterranean lifestyle. Those big front paws, in particular, are used for digging tunnels into the soil. Aside from being large relative to the rest of its body, the paws also have an elongated and enlarged radial sesamoid bone just beside the thumb. In some species of mole, this false 'thumb' (although it doesn't actually protrude as a distinct digit) is actually capable of some independent movement, spreading outwards to widen the hand.

This same wrist bone is also modified in giant pandas to form their peculiar 'thumb'. The panda uses its false thumb in feeding, to strip down the bamboo shoots that comprise its diet. (A photo of this in action can be found here.) This was the subject of a well-known essay by Stephen Jay Gould that later titled one of his published collections. As an example of what he called 'Tinkertoy evolution', it illustrates how evolution often makes do with existing structures to fulfill new functions. It is examples like these, which are less than perfect and highly contingent functional solutions, that break the illusion of a perfect world as posited by natural theology, and demonstrate evolution in action, he argued. (It's also the name of a popular evolution blog.) 

The case of the mole's 'thumb' also bears out this theme. Developmental biologists have recently found that Sox9, a gene involved in limb chondrification (the formation of cartilage tissue), is expressed in the region of the enlarged radial sesamoid during the development of the front paws of a mole embryo. This gene is also expressed in the 'normal' developing digits. However, the timing is different: it is expressed in that region of the wrist after Sox9 expressed has faded away in the normal digits. They compared this pattern of gene expression in embryos of the shrew, which are the closest relatives to moles, and did not find any Sox9 expression in the wrist at the same developmental stages.

Therefore, similar developmental mechanisms (the 'toolbox') have been co-opted to form the mole's false thumb, but their timing has been changed. That seems an easier option than to invent an entirely new set of tools.

Instances of obvious 'tinkering' such as this one make the messiness of evolution more apparent to us. Even structures of of evident perfection such as the eye (or eyes, since image-forming eyes have evolved multiple times) evolved by a long process of making do with existing structures to form new ones (clip from the BBC science show 'Bang Goes the Theory'). After all, isn't this just descent with modification, the very concept of biological evolution itself? Even at the level of genes and genomes, new genes often originate by duplication of existing genes (or even entire genomes, in the phenomenon of polyploidy) followed by divergence in function of these new copies from their originals. A whole book has recently been published on this subject.

What intrigues me is that the evolution of language also seems to have a similar pattern, and not just in terms of coining new words or borrowing vocabulary from other languages, but in the very grammatical structure of a language. Apparently 'perfect' systems like the Latin noun cases are actually the intermediate products of an ancient and on-going process of decay, accretion, and modification. A readable account is found in a popular-linguistics book I recently read, The Unfolding of Language.

Perhaps I'm straying too far from the original point of this post, and making a mountain out of a molehill, but the parallels to be found throughout the natural world and between the different sorts of evolution, biological and cultural, continue to fascinate me. Nature has immense and dizzying diversity, but that doesn't mean it has to be opaque to our understanding. 

Sources:

• BBC News story by Jennifer Carpenter
• C Mitgutsch et al. (2011) Circumventing the polydactyly 'constraint' - the mole's thumb. Biology Letters published online 13 July 2011. doi: 10.1098/rsbl.2011.0494

Islamic creationism in Malaysia

Salman Hameed is an astronomer and sociologist of science at Hampshire College in the US. He has been conducting an extensive survey on Muslim attitudes to science and religion in several Muslim-majority countries around the world.

"[Hameed] has found that attitudes about evolution vary greatly from country to country. For instance, most Pakistani doctors accepted evolution, even human evolution. "But in Malaysia, we were really surprised to find a major rejection of not only human evolution but evolution in general," he says.

"Hameed expected to find more acceptance of modern science because Malaysia has a sophisticated high-tech industry. He and his colleagues now speculate that Muslims are trying to carve out a cultural niche that's distinct from the more educated Indians and Chinese in Malaysia. "We think the rejection of evolution has become part of their Muslim identity," he says."

(Source: Chronicle of Higher Education)

The article goes on to discuss other findings that were presented at a symposium on Islam and science held at Cambridge University this past May. One of the major figures in the world of Islamic creationism is Harun Yahya from Turkey, the pen name of Adnan Oktar. A previous blog post here on creationism in Hong Kong schools mentioned him in passing. He was responsible for sending a hefty, full-color tome titled the Atlas of Creation to major universities and research institutions world-wide, to the amusement and befuddlement of academics and scientists who received them. He has an extensive media empire publishing creationist titles, but a profile in the New Scientist magazine suggests that politics are also at play.

The apparent growth of creationism in Malaysia is as much a sociopolitical issue (of "identity politics") as it is a scientific one. Therefore the standard solution of "more education" on its own may be insufficient to overcome this obstacle to promoting scientific and technical literacy in the country.

"Mismeasure of Man" Revisited

Stephen Jay Gould's 1981 book, The Mismeasure of Man, made the case against 'scientific racism'. He opened the book with an attack on the 19th-century physical anthropologists, the craniologists, who measured skulls as a way to classify different races as superior or inferior. Later on, he examined the origins of the IQ test and argued against its validity and statistical basis. In 1996, the book was reissued with a set of new essays, in response to the controversial 1994 book The Bell Curve. This was welcomed by those who opposed the Bell Curve's revival of biological determinism in intelligence.

Fifteen years on, Gould's book is back in the news but to criticism, rather than acclaim. One of the bodies of work that he analyzed and apparently refuted was that of Samuel George Morton, an American craniologist who amassed a large collection of skulls from around the world. Gould claimed that Morton's measurements exhibited bias, unconscious or not, that bolstered the preconceived notion that Europeans should have larger brain volumes than other, 'inferior' races. Morton supposedly fudged his analysis by selective reporting (see my previous blog post on other ways to fudge your science) and improper measurement. However, Gould did not remeasure the skulls himself, basing his criticism only upon his re-analysis of the published data. Now, a study by anthropologists who painstakingly remeasured Morton's skull collection has absolved Morton of misconduct. There was no mismeasurement, contradicting Gould's thesis that unconscious bias had influenced Morton's scientific methodology. The research team says: "Ironically, Gould's own analysis of Morton is likely the stronger example of a bias influencing results."

Read more at the New York Times, and the original article in PLoS Biology.

Reference:
Jason E Lewis et al. 2011. "The Mismeasure of Science: Stephen Jay Gould versus Samuel George Morton on Skulls and Bias." PLoS Biology 9(6): e1001071. doi:10.1371/journal.pbio.1001071

"Primitive" fungi discovered... in a pond!

The microbial world is ubiquitous (there are microbes everywhere!) and vast (there remains so much to be discovered). Basic discoveries are made on a fairly regular basis, and new taxonomic groups of microorganisms are routinely identified when people sequence DNA from the environment.

We don't necessarily have to go to exotic locations like hot springs or the deep sea to discover something new. A new group of "primitive" fungi has recently been described from samples taken from a variety of locations around the world, including a pond in Devon near Exeter University in the UK, where the scientists worked.

This group, called the cryptomycota (not capitalized, because it's not yet officially described according to the rules of taxonomy), has characteristics which make it apparently a 'missing link' between the fungi and other eukaryotic microbes. Sequences of a number of genes place it as a sister group to the rest of the fungi; that is to say, on the family tree of the fungi, it branches off at the very base of the tree.

Although the term "primitive" is often used for groups that fall out at the base of phylogenetic trees, like the cryptomycota, it's important to note that they don't necessarily resemble the ancestors of these groups in every respect. That is to say, just because one branch of your family split off many generations ago from your own lineage, it's not true that this branch more closely resembles your great-great-grandparents. Likewise with other living organisms.

However, in this case, the cryptomycota are called a 'missing link' precisely because they have some characters which were presumed to be present in the ancestors to fungi. They have flagella, which are absent in all 'true' fungi except the chytrids. In fact, chytrid fungi were originally not considered to be true fungi, because they had a flagellated stage in their life cycle. Aside from the cryptomycota, the chytrids are the next-most-basal group of fungi. Furthermore, in every intro biology class we learn that fungi have a chitinous cell wall. These are lacking in the cryptomycota, and presumably also lacking in the precursor to fungi, because it's a feature that's unique to the 'true fungi'.

Fluorescence microscopy image of cryptomycota. Flagella are labeled with an antibody (red), the nuclei with a fluorescent stain (blue), and the ribosomal RNA labeled with an in-situ hybridization probe (green). Via BBC News.

As before, it's important to point out that the term 'missing link' is often misinterpreted. Just as the word 'primitive' has commonsense connotations of being somehow worse off than the 'advanced' species, the same goes for 'missing links'. In the context of systematics, what it refers to is the fact that some species retain traits that are present in ancestral species (either known from fossil evidence or inferred by reconstruction), and their having a mixture of 'derived' and 'primitive' characters provides additional confirmation for how we reconstruct the phylogenetic relationships of these related species.


Also notable is how these fungi were identified. It's fairly routine now to study microbes from the environment without needing to culture them in the lab. Sequences of a well-known gene, such as the ribosomal RNA genes, can be produced from DNA extracted from the environment, and then compared with known sequences in databases, to see 'what's out there'. Novel sequences identified in this way can be related to actual cells under a microscope, by labeling them with probes that specifically target these unique parts of their ribosomal RNA, a method called in-situ hybridization. That's what's shown above in the micrograph, where the probe labeled with a green fluorescent molecule demonstrates that these peculiar flagellated cells were the mysterious fungus-like sequences that the scientists kept finding in environmental samples.

So the lesson here is: There's plenty out there waiting to be found, even in stagnant nondescript ponds! As DNA sequencing gets cheaper and labeling techniques become more convenient, I'm sure that we'll be hearing much more news like this, about cool new microbes that many years ago would have been impossible to identify or classify.


Sources:

Jones et al. "Discovery of novel intermediate forms redefines the fungal tree of life." Nature (published online: 11 May 2011) doi:10.1038/nature09984

BBC News

Human DNA contaminates genome databases

Scientists rely extensively on public databases of genomic sequences, such as GenBank, based in the USA, and the European EMBL. They might use this for detailed and exacting statistical studies of molecular evolution, or for doing a quick search to check whether a sequence they've just amplified is indeed what it is. Most biology students today have done a BLAST search at some point, underscoring the ubiquity and usefulness of these bioinformatics tools.

One big problem that haunts these sequence databases, however, is contamination and mis-annotation. Sequences are not always what they say they are, and scientists who don't carefully check the provenance of their data, or who trust that "because it's in GenBank it should be ok" may find their painstaking analysis to be in vain if they had used the wrong data to start with. While this problem is widely acknowledged, it comes as a surprise, perhaps to hear that nearly 20% of non-primate genomes in public databases have some degree of contamination from human sequences, probably DNA shed from the skin of the very scientists and technicians who prepared the material for sequencing.

Why non-primate genomes in particular? The research team from the University of Connecticut decided to use a particular short (less than 300 bases) sequence in the human genome, called AluY, which is repeated in great numbers and is highly conserved among humans and other primates. Alu elements are retrotransposons and an example of SINEs (short interspersed elements) that make up much of the genome. The AluY subfamily is derived from an insertion event that happened in the common ancestor of primates, and its specificity to primates is a marker of our common ancestry.

This is a creative use of past evolutionary events for tackling what is effectively an applied, technical question. It really helps to know some history!

House Too Small? – Overlapping Genes in Viruses

Protein coding genes are complicated things: the four bases of DNA are arranged into triplet codons, each of which codes for one of 21 (more or less) amino acids, which are strung up in a polypeptide chain, folded into a complex 3-dimensional structure where precise shape and chemistry determines function... It would seem that any perturbation would throw this finely-tuned system off-kilter.

Even more outrageous is the notion that genes can overlap and still code for perfectly functional proteins, because this implies that, for part of the gene at least, a different reading frame still has functional meaning. This flies against our intuition that frame-shift mutations are the deadliest of all, and has been likened to taking a paragraph of text, moving all the spaces between words down by a character, and still being able to read it, but this time with a completely different meaning!

Viruses, though, are capable of this sort of contortion, and a number of hypotheses have been proposed to explain why they find it necessary to do so. Is it a way to reduce the overall genome length in the face of a high mutation rate? Or is it a means to couple together the expression of more than one gene? Looking at a number of viral genomes, a team from Italy and the UK claim to have found the reason: overlapping genes are a response to the constraints placed by viral capsid size.

For viruses that use RNA for their genetic material, there is a known inverse relationship between genome size and gene overlap: the longer the genome, the less gene overlap is present. They confirmed that this also held for DNA viruses. But when they grouped viruses by the kind of capsids they have–icosahedral vs. flexible–they found that this relationship is strong in the icosahedral capsid viruses, but weak in those with flexible capsids. Capsids are protein 'coats' that encase the viral genome; icosahedral capsids are particularly rigid and constrained in size, because their geometric configuration (icosahedra are one of the five Platonic solids of classical geometry) is the result of the interlocking of the protein units that make up the coat. There are precise mathematical rules that govern the assembly of these units.

Icosahedral adenoviruses (electron micrographs) with cartoon of icosahedron. (Wikimedia Commons)

On the surface, it seems like an extreme solution, even reminiscent of the infamous Bed of Procrustes. These viruses appear to have found a way of surviving the ordeal. It's so striking because we wouldn't expect to see what is patently a physical constraint leaving such a distinctive genomic signature, the latter being strictly informational. At the molecular level, though, there may be a fuzzier line between the two.

This is one of those things which writers used to attribute to the 'ingenuity of Nature', but speaking in materialist terms:

"In effect, the capsid poses an engineering problem for the creation of genomic novelty, and gene overlap is the way around it."

The Elephants' New Tree

Top (L to R): African Savannah Elephant, African Forest Elephant, Asian Elephant

Bottom (L to R): Woolly Mammoth, Mastodon

Source: Wikimedia Commons (click through for source pages)

African Elephants have big ears, Asian Elephants have small ears - that's how we usually learn to tell these two apart. The "African Elephant", though, actually comprises two species in the genus Loxodonta, the Savannah elephant (L. africana) and the Forest elephant (L. cyclotis). The Asian elephants are not as closely related as these two, and are in the genus Elephas. Whether the two species of African elephants are really distinct species, however, has been a subject of debate ever since they were first described by zoologists. New research, however, shows that they are indeed different species, and that this divergence is an ancient one. What's more, the Asian elephant is a closer relative to the woolly mammoth than it is to the extant African elephants!

A scientific team led by researchers from the Broad Institute at Cambridge, Massachusetts and the Max Planck Institute for Evolutionary Anthropology in Leipzig have used DNA from the three extant elephant species as well as ancient DNA from the Woolly Mammoth (Mammuthus) and the Mastodon (confusingly called Mammut) to reconstruct the Proboscoidean family tree. What's really novel about their methodology is that they have used tens of thousands of nucleotides of DNA sequence data, spanning several hundred loci (genes) on the nuclear genome of these elephants. Most phylogenetic studies (i.e. research that aims at reconstructing the genealogy of organisms) generally looks at only a handful of genes because large quantities of data are expensive (money-wise) to produce and computationally expensive to crunch through. They took advantage of the Broad Institute's expertise in next-generation pyrosequencing, where DNA is "sequenced by synthesis", based on technology that is fundamentally different from the decades-old Sanger sequencing technology that we learn about in school.


Their results are based on nuclear genes, but show a conflict with previous results obtained by analyzing the mitochondrial genome (mtDNA) of these elephants. mtDNA suggests instead that the African elephants share a relatively recent common ancestry, within the past half-million years or so. What could be happening is that mitochondrial and nuclear genomes are evolving under different circumstances, because the mitochondria are inherited only through the maternal line. The authors hypothesize that this difference is caused in part by the matriolcal behavior of elephants - matriarchal herds stay more or less in the same place, while waves of male migration spread out and fertilize herds elsewhere, displacing nuclear genes but not mitochondrial ones.


The value of ancient DNA is now well-recognized, and has entered the mainstream in science, where previously it tended to be viewed askance as a fringe endeavor more associated with science fiction than real science (think Jurassic Park). What I'd like to see this research group do in the future is to obtain sequences from a larger pool of animals. At present they have DNA sequences from only one or two individuals of each species. A larger data set would allow us to see how well-supported the nuclear-mtDNA divergence really is, and what degree of variation is present at the populational level for this species. As sequencing costs and computational costs go down, it will certainly be cheap enough, one day, to do large-scale population genetics at hundreds of loci. Also, it would have been valuable to see what tree topologies they would obtain using other tree-building methods, because neighbor-joining is known to produce branch lengths that are difficult to interpret, and information is lost when compressing data into distance metrics.

Egyptian crypt aids search for origin of dogs

One of the most charming and enjoyable books about dogs is Man Meets Dog by Konrad Lorenz, who was one of the founders of the field of ethology, or the scientific study of animal behavior. This book popularized ethology but unfortunately one of Lorenz's other theories, that dogs were descended from jackals, has been found by more recent scientific work to be wrong. Dogs are most probably descended from wolves, which seems mind-boggling if we look at the tremendous variety of dog breeds. How did they all come about?

It is in this context that the rediscovery of a crypt for dog bones in Saqqara, Egypt is significant. These animals were sacrificed upon the death of their owners, and were entombed underground, sometimes mummified. Although ancient Egyptians were known for their love of cats, there was a significant interest in dogs and dog-breeding among them too. This crypt therefore preserves for us, like a snapshot in time several millennia ago, a cross-section of dog variation in the course of their domestication that may give some insight into the evolution of modern breeds, and their origin from wolves.

Book Review: The Art Instinct

Book reviewed -- Denis Dutton. The Art Instinct. New York: Bloomsbury Press. 2009.

Modern humans have a profound fascination with our Pleistocene past, in part because many of us, disillusioned by technology and modernity, find something more authentic and natural in the ways of hunter-gatherers. A recent post by fellow Refugee, Alvin, highlights research suggesting that barefoot running may be better for our bodies. For some people, the 'Paleolithic Diet' is becoming fashionable, while even literary theorists are looking to Darwin and the hunter-gatherer psyche to explain the ins and outs of literature. Can other human endeavors, like art and music, be explained by our evolutionary past in the same way?

Tuataras!

Natalie Angier, a science writer at the New York Times, has written a great feature article on the tuatara, a 'living fossil' that is the only remaining representative of its group, the sphenodontids. All other lizards and snakes are members of a group called the Squamata, which is distinct from the Sphenodontidae (see a reptile phylogeny at Tree of Life).

Some fun facts include their 'third eye' (the pineal eye), a primitive light-sensing organ in the center of their head which has been lost in most living reptiles, and their longevity - individuals in the wild may routinely reach 100 years or more, and continue to reproduce despite their advanced age.

Her article highlights research that shows how certain parts of the tuatara genome are evolving at a rapid rate, despite their apparent morphological 'stasis'. This questions our popular notion of what a 'living fossil' is - although they may appear to be quite similar to fossilized relatives from millions of years ago, we shouldn't forget that these organisms have had corresponding millions of years of evolution since that time, and so morphological stability may conceal other advanced specializations. It would be a mistake to think of these organisms as 'primitive' in the common sense of backward and inadequate.

RIP, G.C. Williams

The American biologist George C. Williams has died at the age of 84. Williams worked and taught for a long time at SUNY Stony Brook, and is best known for his book Adaptation and Natural Selection, published in 1966, where he criticized the idea of 'group selection', which can be caricatured as the idea that traits evolve 'for the good of the species'. He emphasized how natural selection can only act on individuals; his book was one of a clutch in the 1960s that led to the formulation of the gene's-eye view of natural selection. This change of perspective would bring evolutionary thinking back to the basics of selectionism and population-thinking, as first proposed by Darwin.

These are topics that are standard fare in any biology or evolution course today, so it is with some difficulty that I first appreciated its importance when reading his book. It's a problem that my roommate, a big movie buff, complained about in a different setting: when he watched a classic Western for the very first time, he thought that it was cliched and boring, using all the tropes and tricks found in every Western outlaw film. Why did people say that it was such a great movie, then? Because it was the first to do these things, and all the other films in the genre since then have been imitating it. A similar situation awaits the modern reader of Adaptation - we've been steeped so thoroughly in the gene's-eye view by popular science writers such as Richard Dawkins, so much so that we might think that Williams's book is just stating the obvious. In the early 1960s, though, biologists could still seriously speak of groups or whole populations as having adaptive traits, i.e. that natural selection could work at the level of the group. The demolition of this so-called 'group selection' was so complete that even today the term still has a whiff of taboo. The anthology Group Selection published in 1971, and edited by Williams, gives a good overview of the transformations in biological thinking during this period, through selections from the original literature.

Williams is also known for his theory of aging, or senescence. Growing old is a problem, not just for people, but for science. Why should an organism age? Why not be immortal? Wouldn't a gene for immortality be selected for? He explained it in evolutionary terms as a trade off - suppose a given trait allowed the individual to be more fecund earlier in life, but at a cost to it when it grew older. That trait would be selectively favored, because in a natural setting, the probability of reaching old age is low given the pressures of predation and the harsh environment. If you knew that you were going to die young, wouldn't you empty out your bank balance, too? This observation is borne out in humans, as modern medicine has allowed us to increase our lifespans way beyond what we would expect to live in the wild. As a result, so-called 'diseases of aging' are becoming ever more prevalent. In the mid-1990s, Williams and a medical doctor, Randolph Nesse, collaborated on a book that explored just this topic for a general audience, Why we get sick: The new science of Darwinian medicine. It was indeed a new science, which even today is still experiencing growth, but it traced its beginnings to Williams's theory of aging which he first proposed in the 1950s.

Aside from his original writings, Williams also served editorially at the Quarterly Review of Biology - the main book review for the biological sciences - for over forty years. He was not a flashy popularizer in the mold of Dawkins or Stephen Jay Gould, but his books remain readable and very relevant today. They are still among the best introductions for general audiences or biology students to gene-centered thinking, which has become populated by modelers and theoreticians to the extent that the basic biology can be obscured. In science, primary sources and original writings often become obsolete - because important ideas are repackaged and worked over and sometimes even overturned. It then becomes unnecessary to go back to the original publication because it doesn't necessarily improve your understanding. To understand newtonian mechanics, for example, one doesn't read the Principia but instead the latest version of some college textbook which (hopefully) incorporates refinements in our understanding and pedagogy that have been accumulated in the centuries since Newton. For biology, though, and with Williams in particular, the philosophical nature of these changes in theoretical framework, and their frequent subtlety, make the original texts worthwhile to read, and certainly even today can still stimulate renewed debate and appreciation.

Obituaries:
Chronicle of Higher Education
Edge Magazine
Wikipeida article

Fossilized leaf-mimic lacewings

Lacewings, or Neuroptera, are a order of insects with very distinctively patterned wings, as their names (both in English and Latin) suggest. Among insects in general, many species, especially the well-known leaf katydids, are mimics of flowering-plant leaves. Such leaf mimicry presumably is a form of camouflage that functions in either defence or in aid of predation.

Paleontologists working in China have discovered a rare set of lacewing fossils (open access article) from Middle Jurassic rocks at a site in Inner Mongolia which are leaf mimics - a useful adaptation given their large size. However, their age means that they pre-date the Cretaceous radiation of flowering plants. The relationship between flowering plants (angiosperms) and insects has been characterized as a synergistic adaptive radiation - both groups flourished in diversity on similar timescales, an observation explained by pointing to the frequent close relationships and associations between insects and angiosperms. Therefore, leaf mimicry has long been thought to be a post-angiosperm phenomenon, and virtually all known leaf-mimics pretend to be angiosperm leaves. These lacewings, however, appear to mimic cycads or bennettiales, both of which are non-flowering seed plants (gymnosperms) that dominated the pre-angiosperm plant world. Both fossil and extant cycads have distinctive pinnate leaves, which the lacewings resemble. These are very different in form from the typical angiosperm leaf.

On the whole this is a very neat story - close insect-plant associations or coevolution appeared long before the rise of the angiosperms. The change in plant communities from gymnosperm-dominated to angiosperm-dominated, however, would have diminished the effectiveness of these cycad mimics, and might explain their disappearance. Perhaps some later fossil discoveries, likely coming from China, the new hot-bed for paleontology, might shed more light on the affair....

Down with Kin Selection?

Oecophylla weaver ants in Gombe. Photo by Axel Rouvin via Wikimedia Commons.

The concepts of kin selection and inclusive fitness are centerpieces of modern evolutionary biology. Almost every biologist has some familiarity with at least the outline of the issue, and they are staples in textbooks and in the classroom. Briefly, these ideas were introduced in the mid-20th century to explain the apparent paradox of how altruism and cooperation might evolve in a biological system. If natural selection favors the spread and fixation of genes that cause an individual to have more offspring, how can we explain the evolution of traits which involve one individual aiding another at some cost to itself?

Cooperation might seem to be intuitively beneficial, but consider a population of animals which all sacrifice a bit of their potential individual fitness in order to cooperate for some greater good, e.g. defending the nest from predators. They will get good returns on their investment if they all cooperated honestly. However, such a group is prone to invasion by so-called 'cheaters', which take but do not give back. A group of cooperators without defences against cheating will rapidly be overtaken by cheaters, and hence any cooperative endeavour is doomed to crumble.

It was to resolve theoretical problems like these that the idea of inclusive fitness was introduced. Individual fitness is simply the number of offspring that one produces. Inclusive fitness, on the other hand, counts not just one's own offspring, but the offspring of relatives, multiplied by the factor of relatedness. The process by which it functions is kin selection - if one helps one's relatives and contributes to their individual fitness, then one is contributing to one's inclusive fitness. A gene for cooperation could hence spread and be resistant to cheating, because it is more likely to be present in relatives of an individual that already bears that gene, than in unrelated individuals. The essence of the idea is found in a prescient quip by the geneticist JBS Haldane, who said that he "would [lay down his life] to save two brothers or eight cousins" (Wikiquote) - because the relatedness (more rigorously, the probability that a gene is identical by descent) of siblings is 1/2 and that of cousins is 1/8.

A new look at the math (the derivations are in the supplementary material, but the main paper is unfortunately hidden behind a paywall) behind inclusive fitness theory is now claiming that it is no better than standard natural selection theory in explaining one of the key problems of biology, the evolution of eusociality (edit 28/8/2010: Harvard Gazette press release). The group, comprising mathematical biologists Martin Nowak and Corina Tarnita, and the father of sociobiology EO Wilson, explain that inclusive fitness is merely a different way of 'doing the accounting' which is somewhat more complicated than it needs to be. That is, it is too specific, relying on certain assumptions (additive fitness effects, pairwise interactions only, weak selection) which are fulfilled in only a few exceptional cases. It is not an adequately general theory, in the mathematical sense of the word. They also challenge the validity of Hamilton's rule, the simple-looking equation that states that a gene for a cooperative behavior will spread if:

Relatedness > cost/benefit

Population biologists trying to test Hamilton's rule in actual organisms have found it difficult to measure these quantities. The authors of this paper, using a more explicit derivation, found that cooperation does spread when something is greater than the cost to benefit ratio, but this 'something' (as they put it) is not relatedness. In place of inclusive fitness theory, they propose that the more general game-theoretic theory of natural selection, used in conjunction with precise models of population structure, is adequate to explain the evolution of cooperation, without invoking kin selection.

What then, of the crown jewel of kin selection, the explanation of eusociality in hymenopterans? Hymenopterans are the insects which include bees, wasps, and ants. They have an unusual genetic system called haplodiploidy: females lay either fertilized (diploid) or unfertilized (haploid) eggs. The former hatch into females, and the latter into males. The ants are perhaps the most successful and best known eusocial animals. Kin selection theory explains the cooperation between female, sterile worker ants (who might easily defect and start laying eggs of their own) in terms of their relatedness - sisters are more closely related to each other (relatedness of 3/4) than daughters are to mothers (1/2), and so cooperation among sisters can spread. Not all eusocial animals have haplodiploid sex determination - termites, for example, do not. As more eusocial animals have been found, it turns out that the number of haplodiploid lineages is in the minority. An alternative explanation has to be found for eusociality, because the kin-selection based explanation as given above was now most probably an exception to the rule.

Naked mole rats are eusocial mammals. Photo via Wikimedia Commons.

Ed Wilson has proposed for some time now that eusociality is to be explained by theories other than the traditional haplodiploid hypothesis (in Quarterly Rev. Biol., Bioscience (pdf), PNAS) . Briefly summarizing, his model, which is adopted and refined in this paper, involves the formation of groups subject to selection, the predisposition to group-formation by certain 'preadaptations' (they cite the example of solitary bees being behaviorally programmed to complete tasks in sequence - hence they naturally divide labor when forced to cohabit), and selection acting at multiple levels. Hence organismal traits and population structure are sufficient, without having to invoke the concept of inclusive fitness.

This analysis is quite satisfying because it represents the convergence of two different approaches to population biology: that rooted in mathematical theory and that rooted in natural history. The strong claims that it makes will certainly trigger robust debate. However it turns out, it will be interesting to see how the study of eusociality will respond. As the authors note (quite provocatively, given the highly charged reception to the original publication of Sociobiology in the 1970s), "[w]e have not addressed the evolution of human social behavior here, but parallels with the scenarios of animal eusocial evolution exist, and they are, we believe, well worth examining."