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The May Origins essay examined the origins of the immune system but focused exclusively on the microbial defenses animals use. Here, Claire Thomas examines what scientists are learning about the evolution of plant immunity—and whether there are any connections with animal immunity.

Most of us know the basics behind the “adaptive” immune system in mammals—thanks to school biology lessons about white blood cells that specifically attack and engulf pathogens or make antibodies that grab those microbes—but how do plants protect themselves?

At first glance, plant immunity is far simpler: Plants rely partly on their rigid cell walls to keep out microbes. They don’t have a circulatory system and therefore no roaming immune cells to track down bacteria and viruses. But they do have one fundamental thing in common with mammals: a basic “innate” immune system. In mammals, the white blood cells that make antibodies or specifically target microbes rise up only after this innate arm carries out the initial immune response to a pathogen, typically causing inflammation. Plants, on the other hand, can only use their innate responses to fend off pathogens.

But as scientists have compared plant and animal immunity, they’ve been struck by something surprising. “The current evidence and belief is that there is tremendous similarity between animal innate and plant immune systems,” says Dan Klessig, a plant pathologist at Cornell University. In fact, both systems use similar receptors to detect invading pathogens.

Which raises an intriguing issue: Did a primordial ancestor common to plants and animals evolve a basic innate immune system, which began to differ in the two lineages once they split (divergent evolution)? Or did plants and mammals evolve innate immunity independently but end up with similar mechanisms (convergent evolution)? That’s something that scientists have puzzled, and argued, over. “It’s an area where there’s more debate than data,” says plant geneticist Peter Tiffin of the University of Minnesota, Twin Cities.

brainart

The nervous systems of modern animals are amazingly diverse. A few hundred nerve cells are all a lowly nematode needs to find food and a mate. With about 100,000 neurons, a fruit fly can perform aerial acrobatics, dance to woo a mate, and throw kicks and punches to repel a rival. The sperm whale’s 8-kilogram brain, the largest on the planet, is the navigation system for cross-ocean travel and 1000-meter dives and enables these highly social creatures to communicate. The human brain—one-sixth that size—is the wellspring of art, literature, and scientific inquiry.

In this month's Origins essay, Greg Miller takes a look at how nervous systems got started. He investigates what the first neurons might have looked like and what advantages they conferred on the animals that possessed them. These were questions the father of evolution, Charles Darwin, was ill-equipped to address. Only around the time Darwin died in 1882 were scientists beginning to develop stains to label individual cells for detailed postmortem neuroanatomical studies. Methods for investigating the electrical properties of individual neurons in living brain tissue were still decades away, to say nothing of techniques for investigating genes and genomes. Using such modern tools, scientists have recently begun to gain some tantalizing clues about the evolutionary origins of nervous systems. By looking down the tree of life, they are concluding that assembling these components into a cell a modern neuroscientist would recognize as a neuron probably happened very early in animal evolution, more than 600 million years ago. Most scientists agree that circuits of interconnected neurons probably arose soon thereafter, first as diffuse webs and later as a centralized brain and nerves. But the resolution on this picture is fuzzy. The order in which early branches split off the animal tree of life is controversial. And Miller takes a look at the different story lines implied by these different arrangements.

—Elizabeth Pennisi

Illustration: Katharine Sutliff

sexartSex gives nature much of its spice. Fireflies flash through the night to find mates; a flower’s perfume lures insects to carry pollen to distant partners; male bullfrogs croak to impress females. Currently, biologists understand the molecular nuts and bolts of sex fairly well. But the why of sex is still fairly mysterious. Bacteria don’t have to search for mates; they just grow and divide in two. An aspen tree can simply send out shoots that grow into new trees. No muss, no fuss with finding a partner, fertilizing an egg, and joining two genomes.

Darwin felt the whole subject of sex was "hidden in darkness.” In this month's Origins essay, Carl Zimmer sheds light on sex with his examination of progress since Darwin's day in understanding the "why." Today, scientists use genomics and other 21st century tools to search for answers. They are finding hidden signs of sex in the DNA of supposedly asexual organisms and are tracking the evolutionary impact of sex among living populations of animals and plants. Some use sophisticated mathematical models to assess the conditions under which sex can arise. These efforts are providing new hints about how sex first emerged some 2 billion years ago and about the forces that have made it so widespread. The new studies bolster a handful of hypotheses: Sex may speed up evolution, for example, or it may provide a better defense against parasites. In the past, scientists have focused on just one of these hypotheses at a time, but today many argue that several forces may be at work at once.

—Elizabeth Pennisi

Credit: DEA Picture Library/Getty Images

sea lamprey (Wikipedia)

The sea lamprey draws attention mainly for its alienlike appearance, particularly its oval mouth ringed with rows of sharp teeth that allow the parasitic creature to latch onto a fish host. These eel-like creatures are often called “living fossils” because they are thought to have changed little since they arose 450 million to 500 million years ago, as part of a branch of jawless creatures that split off early from the rest of the vertebrate tree. Lampreys and hagfish are the only survivors of that jawless branch, and accumulating evidence indicates that the animals have developed an immune system far different from that of other vertebrates, including people. Today, in Nature, a team led by Max Cooper of Emory University in Atlanta, Georgia, unveils the latest chapter in this emerging evolutionary tale, providing data indicating that the sea lamprey has its own versions of B and T cells, the two cell types central to the so-called adaptive immune response found in people. Whether those lamprey cells are related to our T and B cells, or are an independent invention, remains unclear, but that hasn’t dampened the fascination of immunologists. “I don’t think there’s any question now that there’s a separate adaptive immune system in the lampreys,” says Chris Amemiya of the Benaroya Research Institute at Virginia Mason in Seattle, Washington.

This month’s Origins essay tackled the evolution of the immune system, but it took a decidedly parochial view of the topic, focusing primarily on the microbial defenses wielded by people and other jawed vertebrates. The essay didn’t describe the lamprey story, which first gained prominence several years ago.

Now a Ph.D. student in evolutionary biology, Nicholas J. Matzke was a public information officer at the National Center for Science Education (NCSE) back in 2005. As such, he played a key role in NCSE’s participation in the Kitzmiller v. Dover Area School District trial that pitted intelligent design (ID) proponents against supporters of evolution. In particular, Matzke was central to the trial’s focus on the evolution of the immune system and the cross-examination of ID proponent Michael Behe. He recalls that episode, described in this month’s Origins essay looking at the evolution of the immune system, in an e-mail interview (edited for clarity) with Science's John Travis.

Q: Was it obvious to make the origin of the immune system a focal point of the case? I read that previous online debates with ID proponents led to the choice.

N.M.: Yeah, partially. The fuller story is that for several years, 2001-2004 or so, a number of us "Internet creationism fighters," of which I was one (as a hobby, before I worked at NCSE), would get on various UBB bulletin boards and newsgroups (and blogs starting in about 2004) and debate the ID guys. We were the people associated with TalkOrigins.org, TalkDesign.org, etc. (Later, this group became the Panda's Thumb bloggers.) Anyway, these debates were long and covered just about every topic in more detail than almost anyone could want. After doing this for years, we got a sense of not just where and how the IDists were wrong (since they are wrong on just about everything), but areas where they are spectacularly, obviously, blatantly, embarrassingly wrong. E.g., Behe's irreducible complexity (IC) argument is the favorite ID argument. And it is true that in 1996, some of the biochemical systems Behe used as examples had not received much attention in terms of their evolution. However, the immune system had received lots of attention even in 1996, and much more by 2005, primarily because (1) it is medically crucial, so there are many more researchers/funding/studies on it, and (2) much of immunology going back to the beginning has relied on comparative studies in animals, so there has been an explicit evolutionary context for 100 years in that field.

The amount of work is relevant because the IC argument always goes like this: 1. ID guy: Natural selection can't explain an IC structure because all of the parts would have to come together at once. 2. Evo guy: Here are some systems with only some of the parts but they still have some function, so your argument doesn't work. 3. ID guy: That doesn't explain how these systems arose, we need to see peer-reviewed publications giving detailed, testable explanations. 4. Evo guy: Here is a peer-reviewed publication on the topic. 5. ID guy: It's not detailed enough, I need to see every single mutation and selection event detailed or I will still say that ID was responsible, not evolution.

At this point, the ID guys have (a) given up on their original IC argument and (b) demanded an impossible, ridiculous amount of detail for the evolutionary explanation, while providing no details or tests of their own explanation. It looks ridiculous from the outside, but ID guys, including Behe, made these moves so regularly that it was pretty predictable.

So, in 2002 this began to become obvious when Matt Inlay wrote it up in an essay for talkdesign.org ("Evolving Immunity"). We then jumped Dembski with it in 2002 or 2003 on his own Internet forum at iscid.org and observed the above progression. Then we posted a bunch of references to articles on the topic and challenged Dembski to provide as much detail for the ID explanation. Here was Dembski's response:

"ID is not a mechanistic theory, and it's not ID's task to match your pathetic level of detail in telling mechanistic stories."

A similar episode happened with Behe in 2005.

In spring 2005, Eric Rothschild began preparing for Behe's deposition in the Kitzmiller case, which was happening in May. I gave him all this background and said if we wanted to pick one system to challenge Behe on, it should be the immune system. We poked him a bit on it at the deposition and got the expected replies.

So then, before the trial, I assembled the stack of books (from the UC Berkeley biosciences library) and articles on the evolution of the immune system and made a big exhibit for Eric to use. Eric asked the questions and got the expected replies, so when Behe started making noises about how the science "wasn't detailed enough," Eric started piling books and articles on the stand, and asking Behe if it was good enough for him. The rest is history...

Q.: You have called the Behe cross-examination on immune origins a "turning point" in the trial. Why do you say that?

N.M.: Well, it was kind of the ultimate Behe defeat amongst a long string of defeats during the Behe cross. I think Eric's whole cross was a "turning point" in that Behe's direct testimony was the one big chance the defense had to come back after the plaintiffs had been beating on ID for 3 weeks during the plaintiffs' case.

It was kind of a turning point for the whole ID argument over the last decade or two because it really exposed for all to see that ID was mostly boasting and dissembling, compared to the substance (physical substance, in the case of the immune system exhibit!) of the evolutionary science.

It was very gratifying to have my very obscure hobby turn into a key skill in an internationally recognized court case. It was kind of like the movie Galaxy Quest, where the Trekkie nerd gets told that the spaceship and aliens from the Star Trek-esque TV show are all real, and his nerdy knowledge saves the day.

In our initial Origins essay looking at the origin of life on Earth, Carl Zimmer discussed research on how the key genetic molecule RNA may have arisen from an abiotic broth. Part of the discussion centered on the RNA work of John Sutherland of the University of Manchester in the U.K., some of which is being published today in Nature. Here's the relevant excerpt from our essay:

Step 1: Make RNA
An RNA molecule is a chain of linked nucleotides. Each nucleotide in turn consists of three parts: a base (which functions as a "letter" in a gene's recipe), a sugar molecule, and a cluster of phosphorus and oxygen atoms, which link one sugar to the next. For years, researchers have tried in vain to synthesize RNA by producing sugars and bases, joining them together, and then adding phosphates. "It just doesn't work," says Sutherland.

This failure has led scientists to consider two other hypotheses about how RNA came to be. Cleaves and others think RNA-based life may have evolved from organisms that used a different genetic material—one no longer found in nature. Chemists have been able to use other compounds to build backbones for nucleotides (Science, 17 November 2000, p. 1306). They're now investigating whether these humanmade genetic molecules, called PNA and TNA, could have emerged on their own on the early Earth more easily than RNA. According to this hypothesis, RNA evolved later and replaced the earlier molecule.

But it could also be that RNA wasn't put together the way scientists have thought. "If you want to get from Boston to New York, there is an obvious way to go. But if you can't get there that way, there are other ways you could go," says Sutherland. He and his colleagues have been trying to build RNA from simple organic compounds, such as formaldehyde, that existed on Earth before life began. They find they make better progress toward producing RNA if they combine the components of sugars and the components of bases together instead of separately making complete sugars and bases first. Over the past few years, they have documented almost an entire route from prebiotic molecules to RNA and are preparing to publish even more details of their success. Discovering these new reactions makes Sutherland suspect it wouldn't have been that hard for RNA to emerge directly from an organic soup. "We've got the molecules in our sights," he says.

Sutherland can't say for sure where these reactions took place on the early Earth, but he notes that they work well at the temperatures and pH levels found in ponds. If those ponds dried up temporarily, they would concentrate the nucleotides, making conditions for life even more favorable.

Were these Darwin's warm little ponds? "It might just be that he wasn't too far off," says Sutherland.

Today's New York Times has one of the many newspaper articles discussing the study, and it includes a nice graphic that helps explain the new advance.

—John Travis

April's Origins essay in Science is devoted to the evolution of flowering plants and so, too, is a meeting yesterday and today at the Royal Society in London. The finale of the meeting will be an evening public lecture on 12 May, Web cast live and then available archived, by Sir Peter Crane, a former director of the Royal Botanic Gardens at Kew who is now at the University of Chicago in Illinois.

ImmuneEssayIntro With swine flu circulating the globe, it’s appropriate that May’s Origins essay is “On the Origin of the Immune System.” Immunology is the study of how we and other animals defend ourselves against pathogenic microorganisms—bacteria, viruses, and parasites, for example—and this battle goes back to the beginning of evolution. The first multicellular creatures must have had to learn how to be nice to their own cells yet attack any invading cell trying to exploit their resources. Indeed, when biologists look at sponges and other “simple” creatures at the base of the evolutionary tree, they see many of the same microbial defenses that we and other complex animals use, which suggests that at least some form of immunity arose very quickly in the evolution of animals. But those ancient defenses only constitute what scientists call the innate immune response, an all-out molecular and cellular assault on infected tissue. Most vertebrates have a second level of defense, the adaptive immune response, that targets, and remembers, specific microbes. It’s this adaptive immune response, dependent on white blood cells called B and T cells, that physicians elicit when they vaccinate a person against a virus, for example. In a scientific detective story that has played out over the past few decades, researchers have shown how this adaptive immune response arose after innate immunity, and they have teased out the details of the fortuitous event, a random DNA insertion in an opportune spot, that was the key to its birth. The research on this “big bang of immunology” even played a key role in a 2005 trial pitting scientists and educators against those doubting evolution and seeking to diminish its teaching in school systems in the United States.

—John Travis

Illustration: Katharine Sutliff/Science

For some microbes, nickel is a precious metal. A new paper suggests that by starving these bugs, a nickel shortage might have triggered an oxygen surge in the ancient atmosphere. The work will come as good news for researchers who favor an early start for oxygen-releasing photosynthesis, an intensely debated topic that was discussed in Science’s Origins essay for last month.

The oldest photosynthetic bacteria, which lived more than 3 billion years ago, didn’t produce oxygen. But researchers are at odds about when the first oxygen-making bacteria, known as cyanobacteria, appeared. Most experts agree that the early atmosphere didn’t contain significant amounts of O2 until the so-called Great Oxidation Event (GOE) about 2.4 billion years ago. That’s when leftovers of reactions involving oxygen—such as rusted iron deposits—pop up in the geological record. Some researchers assume that oxygen-producing photosynthesizers didn’t evolve until shortly before the event. However, based on evidence such as the balance of carbon isotopes in preserved organic remains and ancient oil thought to be the residue of cyanobacteria, other scientists date the origin of oxygen-generating photosynthesis at 2.7 billion to 2.8 billion years ago—or even earlier.

If the bugs were emitting oxygen hundreds of millions of years before the GOE, why didn’t the gas start accumulating in the atmosphere? One obstacle might have been the microbes called methanogens. Today, these bugs hide from oxygen, sheltering in airless environments such as cows’ intestines, swamps, and landfills. However, they were widespread on early Earth, and the methane they released would have reacted with oxygen from photosynthetic cyanobacteria.

For the GOE to occur, “you need to have a significant decrease in atmospheric methane,” says geologist Kurt Konhauser of the University of Alberta in Edmonton, Canada. And what slashed methane levels by knocking down the methanogens was a shortage of nickel, Konhauser and his colleagues propose in a Nature paper published today.

The researchers scrutinized banded iron formations like these from western Australia (left) Banding Dales Gorge BIF.jpgthat were between 3.8 billion and 550 million years old. These striped sediments record concentrations of different elements in the ancient oceans, so they provide a good indicator of nickel availability. What the researchers found was that nickel abundance dropped by about half between 2.7 billion and 2.5 billion years ago. This decline probably resulted from the cooling of Earth’s upper mantle, which reduced volcanic activity that brings nickel to the surface in eruptions.

Nickel scarcity would have hit methanogens hard because several of their key enzymes require the metal, Konhauser notes. As the microbes’ methane output fell, oxygen levels could rise. “It’s the only explanation that accounts for the big picture,” say Konhauser.

—Mitch Leslie

Source: K. Konhauser et al., “Oceanic nickel depletion and a methanogen famine before the Great Oxidation Event.” Nature 458, 750 (2009).

Photo credit: Mark Barley, University of Western Australia

Origins_waterlilyWhat would our world be like without flowering plants? Some 300,000 species of angiosperms are alive today. Their blooms color and scent our world; their fruits, roots, and seeds feed us; and their biomass provides clothing, building materials, and fuel. And yet this rapid spread and dominance of the terrestrial landscape, which took place perhaps 100 million years go, apparently happened in a blink of geological time, just a few tens of millions of years.

The father of evolution couldn’t quite fathom it. In 1879, Charles Darwin penned a letter to British botanist Joseph Dalton Hooker, lamenting an “abominable mystery” that threw a wrench into his theory of evolution: How did flowering plants diversify and spread so rapidly across the globe? Now, 130 years later, botanists are finally beginning to make sense of what has made this plant group so successful and are sorting out how, and when, flowers got started—and from which ancestor. April's Origins essay, "On the Origin of Flowering Plants," discusses how researchers now have analytical tools, fossils, genomic data, and insights that Darwin could never have imagined, all of which make these mysteries less abominable. Over the past 40 years, techniques for assessing the relationships of organisms have greatly improved, and gene sequences as well as morphology now help researchers sort out which angiosperms arose early and which arose late. New fossil finds and new ways to study them—with synchrotron radiation, for example—provide a better sense of the detailed anatomy of ancient plants. And researchers from various fields are figuring out genomic changes that might explain the amazing success of this rapidly evolving group. Questions still remain, particularly about the nature and identity of the angiosperm ancestor itself. But modern botanists are hopeful that the abominable mystery is well on its way to being solved.

—Elizabeth Pennisi

Credit: Reproduced with the kind permission of the Director and the Board of Trustees, Royal Botanic Gardens, Kew