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Posted by on May 7, 2011 in Nature, Research Blogging, Science | 1 comment

An Unlikely Heroine

By motherhood they were born and by motherhood they lived — life was, to them, just the long cycle of motherhood. — Charlotte Gilman Perkins, Herland (1915)

In 1915, at the height of the American Woman’s Suffrage Movement, Charlotte Gilman Perkins published Herland, a future-set utopian novel in which women, perhaps through divine intervention, acquire the ability to reproduce without men. For one hundred generations they bear only daughters who, in turn, bear yet more daughters.

This vision, an ideal world based on generations of motherhood, became an underlying theme of feminist and lesbian literature throughout the 20th century.  Peaking during the 1970’s Women’s Lib Movement, the feminist library filled with similar utopian worlds where women’s severance from male culture was symbolically finalized when they achieved reproduction without men.

Parthenogenesis is the term coined by esteemed English biologist, Richard Owen in 1849, from the Greek parthenos meaning virgin and genesis meaning birth;  It refers to asexual reproduction through the development of an unfertilized egg.

Among animals there are a number of creatures that reproduce, at least some of the time, via parthenogenesis. Most cases occur in insects and invertebrates –bees, water fleas, and some scorpions, for example. Only about seventy vertebrate species (.1%) are known to reproduce this way, and even then, only under very specific conditions.  The largest such example was a female Komodo dragon (Varanus komodoensis), who, in 2006, surprised zookeepers in the UK by laying viable eggs and hatching young despite never having been with a male dragon. Snakes and smaller lizards have done the same.

But one creature holds the record for eons without sexual reproduction.

From: Who Needs Sex (or Males) Anyway? Gross, L. PLoS Biology Vol. 5, No. 4, e99 doi:10.1371/journal.pbio.0050099

SEM showing variation of bdelloid rotifers and their jaws. (PLoS Biology)

One family, all descended from one mother! She lived to a hundred years old; lived to see her hundred and twenty-five great-granddaughters born … she alone had founded a new race! –Herland

Meet the bdelloid rotifer; a seemingly invincible fresh-water invertebrate that gave up sex (and males) over forty million years ago.  Discovered by Dutch microscope developer and amateur microbiologist Antonie van Leeuwenhoek (1632-1723), the bdelloid (the b is silent) is an unassuming creature, mostly translucent with the consistency and look of a bag of water. She’s made of about a thousand cells putting her just below a human’s range of visibility but large enough to be seen with a decent child’s microscope.

The bdelloid’s elongated body includes structures that allow her to swim, crawl, feel, detect light, eat, secrete waste and reproduce. On her head she sports a retractable wheel-like structure (the corona), which contains her mouth parts. At the other end she has a foot and toes which serve to anchor her firmly to whatever bit of debris she can latch on to. From this secure position the bdelloid waves her open corona, sifting through debris to gobble up smaller microorganisms. When it’s time to move on, the bdelloid wriggles through water with inch-worm-like action or contracts her body, opens her corona, and swim freely to a new location.

“Oh yes,” she smiled. “I do not wonder you are puzzled. We are mothers—all of us—but there are no fathers. We thought you would ask about that long ago—why have you not?”  –Herland

Like the women of Herland, the bdelloid reproduces solely via parthenogenesis, females producing only daughters, each of which mature to bear more daughters. Her reproductive means varies by species; some bdelloids lay eggs and others give live birth to miniature adults. In one Antarctic species up to ten young accumulate inside the mother until she dies, then they are released.  But in the four hundred years scientists have known about bdelloids, no one has ever found a male—and that’s not for lack of looking.  Scientists, trying to discredit the bdelloid’s singular claim to eons of virgin birth, have been searching for any trace of a male; not just in body, but in telltale DNA signs. To date, there is no sign of a father in this long line of mothers.

And this brings up a conundrum.

Antarctic Pond (National Science Foundation)

Most evolutionary biologists agree that while asexual species have short-term advantages (they can reproduce and fill a niche at least twice as fast as a sexual species), they eventually die off because their genome is static. Each a clone of the one before her, asexual animals cannot adapt to changes in their environment. For this reason, most asexual species lived in a single fixed habitat. Over the long haul, sexual reproduction has always been considered the single path to evolutionary success in a changing world.

But the oldest known bdelloid specimens are preserved in amber that dates back 40 million years and the diversity of their gene sequence suggests they are more than twice that age.  Not only that, but bdelloids populate every freshwater environment on earth, from icy Antarctic ponds to murky rainforest swamps. They are able to survive long periods of drought, and can live in areas that are only sporadically wet. (Anyone who has a bird bath or a rain gutter probably plays host to a whole zoo of bdelloids!)

How is this possible?

As I studied these youngsters, vigorous, joyous, eager little creatures, and their voracious appetite for life, it shook my previous ideas so thoroughly that they have never been re-established. — Herland

Under ideal laboratory conditions a bdelloid lives for about 30 days and produces about three dozen eggs or live offspring.  But what about not-so-ideal conditions – those that would confound a normal asexual species?  No problem! Under extreme conditions, the bdelloid simply shrivels up and dries—that’s dries, not dies. Bdelloids, which are naturally aquatic, survive dry spells by desiccating or undergoing a process called anhydrobiosis—and turning into little balls called tuns to wait out the disaster. The tun is not a cyst contained in a hard, protective shell. The creature merely dries up inside its own “skin.” Later, just add water, and voila! A healthy active bdelloid appears. Rehydration can take anywhere from ten minutes to a full day and, according to one source, bdelloid rotifers have been revived after 27 years of sitting dry on a shelf.

 

A bdelloid, in either her active state or her tun state, is indomitable. She is able to withstand as much abuse as nature throws at her and, even more tellingly, as much abuse as science throws at her.  Scientists have relentlessly put bdelloids to the test. Sir Ernest Shackleton, Antarctic Expedition leader, commented in National Geographic, on the efforts of Scottish biologist James Murray to determine the endurance capacity of rotifers:

From: British Antarctic Expedition, 1907-9, under the command of Sir E.H. Shackleton, James Murray

From our point of view there was an element of humor in the endeavors of Murray to slay the little animals.  He used to thaw them out from a block of ice, freeze them up again, and repeat this process several times without producing any result as far as the rotifers were concerned.  Then he tested them in brine so strongly saline that it would not freeze at temperatures above minus 7° Fahr., and still the animals lived.  A good proportion survived a temperature of 200° Fahr. It became a contest between rotifers and scientist and generally, the rotifers seemed to triumph.    –Sir Ernest Shackleton (1909)

More recently scientists have experimented with boiling bdelloids, freezing them to nearly absolute zero (-273°C), and drying them for extended periods.  Bdelloids have been sent up in stratospheric balloons to experience low pressure and temperatures and stratospheric radiation.  In a heroic attempt to push the creatures to their maximum capacity, Eugene Gladyshev and Matthew Meselson at Harvard bombarded bdelloids and sexually-reproducing rotifers with γ-rays from radioactive caesium.  At a dose of 200 Grays (the unit of measure of absorbed radiation), the eggs of the sexual rotifers ended up hopelessly scrambled. But the bdelloids were indifferent and went on to generate the usual number of healthy daughters. At 1000 Grays, their reproduction fell to about 10% but those that could reproduce begat healthy daughters. Compare this to the human response: whole-body exposure to a single dose of 5 Gray of ionizing radiation will kill a human in 2 weeks.

What makes this creature so immune to DNA damage is interesting. It turns out, that the bdelloid genome is self-healing.  David Mark Welch found that the bdelloid genome is  “degenerate tetraploid”, meaning that the creature stores extra copies of genes on four separate chromosomes, rather than two. When one chromosome in a pair is damaged, say by radiation or dehydration, it can repair itself by using its complimentary partner as a template.

Hermit Lichen (National Science Foundation)

Hermit Lichen (National Science Foundation)

This ability to repair their genome allows bdelloids to survive the biggest threat to asexual species: Transposons, rogue snippets of DNA that jump around the genome acting as genetic parasites.  In sexual species these parasites get cleared out when the animals mix up their DNA through reproduction. In asexual species the parasite builds up in subsequent generations until it spells the demise of the entire species. When bdelloids desiccate into their tun form however, their DNA “breaks” and has to be repaired when they rehydrate. This repair cuts out the transposons, allowing the bdelloids to clone clean copies of themselves generation after generation.

Today bdelloid mothers are everywhere. Light enough to be borne by the wind in their tun state, they travel regularly between the African and American continents. They inhabit the Antarctic ice shelf, the Sahara desert, woodland streams, standing ponds, rain gutters, and sewage treatment tanks.  Active bdelloids can be found on wet leaf debris, mushrooms, damp tree trunks, and in mosses and lichens.  Bdelloid tuns have been collected and successfully rehydrated from windsocks, bird nests, feathers and wild animal fur. Somehow, as unlikely as it seems, this tiny spec of a creature has succeeded where all others have failed.

You see, we are Mothers,” she repeated, as if in that she had said it all.   –Herland

ResearchBlogging.org

Welch, D. (2000). Evidence for the Evolution of Bdelloid Rotifers Without Sexual Reproduction or Genetic Exchange Science, 288 (5469), 1211-1215 DOI: 10.1126/science.288.5469.1211

Gladyshev, E., & Meselson, M. (2008). Extreme resistance of bdelloid rotifers to ionizing radiation Proceedings of the National Academy of Sciences, 105 (13), 5139-5144 DOI: 10.1073/pnas.0800966105

Mark Welch DB, Mark Welch JL, & Meselson M (2008). Evidence for degenerate tetraploidy in bdelloid rotifers. Proceedings of the National Academy of Sciences of the United States of America, 105 (13), 5145-9 PMID: 18362354

Caprioli M, Santo N, & Ricci C (2002). Enhanced stress resistance of dormant bdelloids (rotifera). Journal of gravitational physiology : a journal of the International Society for Gravitational Physiology, 9 (1) PMID: 15002563

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