As we observe the 150th anniversary this month of the first publication of Charles Darwin's On the Origin of Species, a new book reviews evolution and ranks the top one hundred most influential species of all time.

Homo sapiens is not at the top of the list.

In fact, we humans, who like to imagine that we are the masters of the universe, don't even rank in the top five.

The most influential species (defined as the species that has most changed life on Earth) is ... the earthworm.

Photo courtesy USDA

"According to Charles Darwin, no living thing has had such a profound impact on history as has the earthworm," says Christopher Lloyd, a history scholar at Cambridge University, UK, and author of What on Earth Evolved?: 100 Species that Changed the World (Bloomsbury, November 2009, $45).

After considering the most important species that evolved before the ascent of human civilization, from the beginning of life on Earth until about 12,000 years ago, and then mulling all the species that have been successful since 12,000 years ago--that is the species that have flourished because of modern humans--Lloyd finds that he agrees with Charles Darwin: The earthworm is indeed the most influential species in the history of the planet.

Descendants of sea worms that existed five hundred million years ago, earthworms came ashore with the first invertebrate invasions of the land, making their living in damp soils broken up by bacteria, fungi and the roots of colonizing plants, Lloyd writes. "These earthworms have been ploughing up the earth, ventilating the soil and nourishing terrestrial ecosystems with their excrement ever since."

The survivors of five mass extinctions, earthworms have had profound impacts on human history, Lloyd says.

"Were it not for their continuous regeneration of soils around damp river valleys such as the Nile, Indus, and Euphrates, early agricultural societies in Egypt, India, and Mesopotamia could never have succeeded in building humanity's first large-scale urban communities." 

"Wherever eathworms plough, people thrive. When worms perish, societies collapse."

Throughout human history earthworms have unintentionally but undeniably triggered the rise of civilizations, Lloyd adds. "Wherever eathworms plough, people thrive. When worms perish, societies collapse."

The European earthworm (Lumbricus terrestris) is probably the most prolific and invasive species in the world, Lloyd says.

"Its success is largely thanks to the spread of Europeans, c. 1600 onwards.

"Immigrant farmers inadvertently brought these earthworms, sometimes called 'night crawlers,' in everything from the soil in their potted plants and their horses' hooves, to the treads of their boots and the wheels of their wagons.

"Today there is hardly a region of North America where Europe's earthworms have not made a home for themselves. There they continue to plough, ventilate and fertilize the soil to the general benefit of life in and on the Earth."

Before Man, After Man

What on Earth Evolved? is divided into two sections--Before Man and After Man. Starting with the early Earth, when loose strands of genetic code swarmed the planet, Lloyd explores the most significant lifeforms that evolved in the deep oceans and then wriggled ashore to become pioneers of life on land. In the second section, the author shows how co-evolution of humans and numerous other key species transformed Earth over the past 12,000 years.

A newspaper science and technology correspondent in a previous career, Lloyd has produced an accessible read, guiding the reader through capsule biographies of a hundred of the most influential species. They include slime, sea scorpions, dragonflies, potatoes, ants, tulips, sheep, dogs, cats, coca, opium, poppies, and grapes.

He ranks the species into a table of influence, revealing those that have most changed life on Earth. Academics will no doubt debate the selection and process, but Lloyd makes a compelling, albeit concise, case for each species. The full list of the hundred most influential species may be seen on the book's Web site, or in the book itself.

Covering all of life in one book would be impossible, of course, but Lloyd has taken an interesting approach to some of the most marvelous products of evolution, leading to renewed appreciation of how much life has succeeded through both competition and collaboration.

Here is Lloyd's top ten most influential species of all evolution:

Evolution's top ten species

1. Earthworm
Made it possible for humans to cultivate the planet, settle, and build civilizations.

2. Algae
Without the countless forms of microscopic algae, larger forms of sea life would never have been able to evolve. All land plants are descended from ancestral forms of algae.

3. Cyanobacteria
Plants, trees, and animals all owe their existence to the presence of oxygen in the atmosphere and oceans, supplies of which were originally established by cyanobacteria, a photosynthesizing bacterium that breaks down carbon dioxide and excretes oxygen.

4. Rhizobia
Organisms capable of "fixing" atmospheric nitrogen into soluble nitrates that fertilize the soil so that plants and trees can thrive.

5. Lactobacillus
Bacteria that live inside the human colon, providing beneficial services such as assistance with digestion of milk and protection against harmful bacteria and organisms such as viruses and fungi.

6. Homo sapiens
Humans did not crack the No. 1 position on Lloyd's list, but we merit five pages in his 416-page book and we are the only mammal in the top 10. We lose points chiefly as a result of our recent evolutionary emergence.

We may not rank as the most influential species in this analysis, but our impact pervades the past 12,000 years as we learned to farm animals and plants and harness mch of the resources of the planet.  In that time humans have had a profound impact on many other species, nurturing those useful to us and driving many that are of little value to us into isolation and even into extinction. Our impact on evolution is clearly in its early phases.

7. Stony corals
Coral reefs are powerful places for the natural conservation and co-operation of species, resulting in the construction of massive undewrwater mountains that house an extraordinary diversity of life.

8. Yeast
It is almost exclusively thanks to the action of this single-celled microscopic fungus that humanity has been able to enjoy everything from leavened bread to fine wine. Some of our best prospects for fuelling sustainable industrialization and transportation in the future are based on ethanol, a by-product of yeast.

9. Influenza
One of humanity's biggest ever killers and still the largest threat to populations on Earth.

10. Penicillium
A naturally occurring antibiotic that has transformed modern medicine and substantially increased human populations.

Bloomsbury Publishing provided a copy of What on Earth Evolved? for this entry.

By James G. Robertson, National Geographic Digital Media

Scientists at the University of Utah have developed an adhesive with many possible medical uses, including repairing bone fractures, based on a glue produced by the sandcastle worm. The announcement was made at the August meeting of the American Chemical Society.

The worm creates a complex water-based mortar to create a home from grains of sand and bits of shell. The adhesive can stick to wet surfaces and doesn't dissolve at certain pH levels, making it ideal for medical applications. Once it has done its job, it can become water-soluble and dissolve.

Photo: A sandcastle worm with beads of its homemade adhesive. Photo by Fred Hayes

The traditional method of healing broken bones by using metal nails, pins and screws is difficult with smaller bones, says Russel Stewart, one of the creators of the synthetic sandcastle worm glue, and scientists have been looking for a suitable adhesive substitute for decades.

"The idea of using natural adhesives in medicine is an old one dating back to the first investigations of mussel adhesives in the 1980s. Yet almost 30 years later there are no adhesives based on natural adhesives used in the clinic," said Stewart in a statement.

Tests are also being done to use the adhesive to deliver other substances to the fracture site, such as antibiotics, pain relievers or molecules that help the fracture heal faster.

So far, the glue has passed toxicity tests and is at least as strong as Super Glue and twice the strength of the sandcastle worm's formula.

Same-sex behavior is a nearly universal phenomenon in the animal kingdom, common across species, from worms to frogs to birds, according to a review of existing research, funded by the University of California, Riverside.

"It's clear that same-sex sexual behavior extends far beyond the well-known examples that dominate both the scientific and popular literature: for example, bonobos, dolphins, penguins and fruit flies," said Nathan Bailey, the first author of the review paper and a postdoctoral researcher in the Department of Biology at UC Riverside.

A female-female pair of Laysan albatross. Females cooperatively build nests and rear young when males are scarce, according to biologists at the University of California, Riverside.

Photo by Eric VanderWerf

However, the review paper points out, "same-sex behaviors are not the same across species," and that researchers may be calling qualitatively different phenomena by the same name.

"For example, male fruit flies may court other males because they are lacking a gene that enables them to discriminate between the sexes," Bailey said. "But that is very different from male bottlenose dolphins, who engage in same-sex interactions to facilitate group bonding, or female Laysan Albatross that can remain pair-bonded for life and cooperatively rear young."

An example of existing research was a study by Sara Lewis, an evolutionary ecologist at Tufts University, published in the Journal of Evolutionary Biology in November, 2008. Read the National Geographic News report about it: Homosexual Beetle Activity Offers Reproductive Edge. The picture above shows two beetles in a homosexual encounter.

Photo courtesy Sara Lewis, Tufts University

Published June 16 in the journal Trends in Ecology & Evolution, the review of existing research by Bailey and Marlene Zuk, a professor of biology at UCR, also finds that although many studies are performed in the context of understanding the evolutionary origins of same-sex sexual behavior, almost none have considered its evolutionary consequences.

    "Same-sex behaviors--courtship, mounting or parenting--are traits that may have been shaped by natural selection."

"Same-sex behaviors--courtship, mounting or parenting--are traits that may have been shaped by natural selection, a basic mechanism of evolution that occurs over successive generations," Bailey said. "But our review of studies also suggests that these same-sex behaviors might act as selective forces in and of themselves."

A selective force, which is a sudden or gradual stress placed on a population, affects the reproductive success of individuals in the population, a UCR news release about the research explained.

"When we think of selective forces, we tend to think of things like weather, temperature, or geographic features, but we can think of the social circumstances in a population of animals as a selective force, too," Bailey said. "Same-sex behavior radically changes those social circumstances, for example, by removing some individuals from the pool of animals available for mating."

Bailey, who works in Zuk's lab, noted that researchers in the field have made significant strides in the past two and a half decades studying the genetic and neural mechanisms that produce same-sex behaviors in individuals, and the ultimate reasons for their existence in populations.

Evolutionary Consequences

"But like any other behavior that doesn't lead directly to reproduction--such as aggression or altruism--same-sex behavior can have evolutionary consequences that are just now beginning to be considered," he said. "For example, male-male copulations in locusts can be costly for the mounted male, and this cost may in turn increase selection pressure for males' tendency to release a chemical called panacetylnitrile, which dissuades other males from mounting them."

According to UCR, the review paper:

• Examines work done to test hypotheses about the origins of same-sex behavior in animals.
• Provides a framework for categorizing same-sex behavior, for example, is it adaptive, not adaptive, occurs often, infrequently?
• Discusses what has been discovered about the genetics of same-sex behavior, especially in the model organism, the fruit fly Drosophila, and in human beings.
• Examines connections between human sexual orientation research, and research on non-human animals, and highlights promising avenues of research in non-human systems.

The reviewers expected the research papers they read for their article would give them a better understanding of the degree to which same-sex behaviors are heritable in animals, UCR said.

Genes vs. Environment

"How important are genes to the expression of these behaviors, compared to environmental factors?" Bailey said. "This is still unknown.

"Knowing this information would help us better understand how the behaviors evolve, and how they affect the evolution of other traits. It could also help us understand whether they are something that all individuals of a species are capable of, but only some actually express."

Bailey recommends that fellow evolutionary biologists studying same-sex behavior in animals adopt some of the research approaches that have been successful in human studies, UCR said.

"We have estimates, for example, of the heritability of sexual orientation in humans, but none that I know of in other animals," he said. "Scientists have also targeted locations on the human genome that may contribute to sexual orientation, but aside from the fruit fly, we have no such detailed knowledge of the genetic architecture of same-sex behavior in other animals."

Bailey and Zuk plan to begin experimentally addressing some of the many issues raised in their review.

Said Bailey, "We want to get at this question: what are the evolutionary consequences of these behaviors? Are they important in the evolution of mating behavior, or do they just add extra 'background noise'?

"We are pursuing work on the Laysan albatross, in which females form same-sex pairs and rear young together. Same-sex behavior in this species may not be aberrant, but instead can arise as an alternative reproductive strategy."

Related National Geographic News stories:

Homosexual Activity Among Animals Stirs Debate

Damselfly Mating Game Turns Some Males Gay

Rattlesnakes Show Strong Family Bonds, Study Says

Homosexual Beetle Activity Offers Reproductive Edge