How the Bdelloid Rotifer Lived for Millennia — Without Sex

As a child, I always wanted a microscope.

I would have collected slimy waters from the scum ponds and murky puddles near my house. I would have brought them home and exposed them to the light of my microscope. I would then have peered deep into a secret world, where shady characters and alien forms lurked and traded.

It would be many years, when I was in college, before I finally witnessed this world—so alien, it might have inspired the science fiction books I wrote later as an adult. As it turned out, I was led to pursue a Masters of Science degree, studying periphyton (microscopic aquatic communities attached and associated with surfaces like rocks and plants) in local streams in the Eastern Townships of Quebec.

Filamentous algae collected in Lake Ontario, ON (photo by Nina Munteanu)

While my work focused on how diatoms (glass-walled algae) colonized surfaces, micro-invertebrates kept vying for my attention. Water fleas (cladocerans), copepods, rotifers, seed shrimps (ostracods) and water bears sang across my field of vision. They flitted, lumbered, wheeled and meandered their way like tourists lost in Paris. But this wasn’t Paris; I’d taken the blue pill and entered the rabbit hole into another world…

Sketch of common zooplankton and phytoplankton (illustration by Nina Munteanu)

The Secret—and Dangerous—World of Micro-Organisms

Small Freshwater habitats are home to a highly productive and diverse collection of micro-invertebrates—multicellular animals that can barely be seen with the naked eye. Many average from 0.5 to 1 mm in size and resemble little white blobs; however, a scholar can distinguish each invertebrate by its unique movement. For instance, when presented with a jar of pond water, I can usually distinguish among the wheel-like wandering of a gastrotrich, dirigible-like gliding of an ostracod (seed shrimp), the vertical goldfinch-style “hopping” of the cladoceran (water flea) as it beats its antennae, or the halting-jerking movements of copepods (oar-feet) as their antennae drive them along like a dingy propelled by an amateur oarsman.

Alas, puddles, ephemeral ponds and vernal pools pose sketchy habitats, given their tendency to appear and disappear in a wink. And like the thief in the night, they pose a harsh and uncertain home to many small organisms. These environments are ever-changing, unstable, chaotic and unpredictable. Yet, anyone who has studied these variable ecosystems understands that they team with life. 

When a puddle or ephemeral pond dries up then reappears with rain, how can these communities thrive? Or do they all die off and then somehow recruit when the pond reappears? Many of these invertebrates have evolved creative ways to survive in very unstable environments. Some form a resting stage—a spore, resting egg or ‘tun’—that goes dormant and rides out the bad weather.

Philodina, a bdelloid rotifer (microscope photo by Bob Blaylock)

Animalcules & the Bdelloid Rotifer

In 1701, Antonie van Leeuwenhoek observed that “animalcules” (likely the bdelloid rotifer Philodina roseaola) survived desiccation and were “resurrected” when water was added to them. He’d discovered a highly resistant dormant state of an aquatic invertebrate to desiccation.

Dormancy is a common strategy of organisms that live in harsh and unstable environments and has been documented in crustaceans, rotifers, tardigrades, phytoplankton and ciliates. “Dormant forms of some planktonic invertebrates are among the most highly resistant … stages in the whole animal kingdom,” writes Jacek Radzikowski in a 2013 review in the Journal of Plankton Research. Radzikowski describes two states of dormancy: diapause and quiescence. (on right: sketch of bdelloid rotifer by Nina Munteanu

Bdelloid rotifers can go into quiescent dormancy at practically any stage in their life cycle in response to unfavorable conditions. Early research noted that dormant animals could withstand freezing and thawing from −40°C to 100°C and storage under vacuum. They also tolerated high doses of UV and X radiation. Later work reported that some rotifers could survive extreme abiotic conditions, such as exposure to liquid nitrogen (−196°C) for several weeks or liquid helium (−269°C) for several hours. Desiccated adult bdelloid rotifers apparently survived minus 80°C conditions for more than 6 years. The dormant eggs of cladocerans and ostracods also survived below freezing temperatures for years.

Rotifers are cosmopolitan detrivores (they eat detritus) and contribute to the decomposition of organic matter. Rotifers create a vortex with ciliated tufts on their heads that resemble spinning wheels, sweeping food into their mouths. They often anchor to larger debris while they feed or inch, worm-like, along substrates. Some are sessile, living inside tubes or gelatinous holdfasts and may even be colonial. Rotifers reproduce by parthenogenesis (in the absence of mates), producing clones (like cladocerans). Resting eggs (sometimes called zygotes) survive when a pond dries up. Bdelloid rotifers don’t produce resting eggs; they survive desiccation through a process called anhydrobiosis, contracting into an inert form and losing most of their body water. Embryos, juveniles and adults can undergo this process. The bdelloid withdraws its head and food and contracts its body into a compact shape called a tun; a generally unprotected dormant state that remains permeable to gases and liquids. Like Tardigrades (see below), Bdelloid rotifers can resist ionizing radiation because they can repair DNA double-strand breaks.

The long-term survival and evolutionary success of bdelloid rotifers in the absence of sex arises from horizontal gene transfer via DNA repair.

In my eco-novel A Diary in the Age of Water the limnologist Lynna visits her technician Daniel as he peers through a microscope and makes the observation of why the bdelloid rotifer is well-suited to climate change:

I bent to peer through the eyepiece at what turned out to be a pond sample in a Petri dish. Attached to a pile of detritus shivering in the current, several microscopic metazoans—rotifers—swung like trees in a gale; they were feeding. Their ciliated disk-like mouths twirled madly, capturing plankton to eat. Watching them reminded me of my early research days as an honours undergrad at Concordia University in Montreal. Probably Philodina, I thought; I had seen many during my stream research in Quebec.

“They’re the future,” Daniel said, looking up at me with a smirk as I straightened.

I raised my eyebrows, inviting him to elaborate, which he cheerfully did.

“They’re the future because of their incredible evolutionary success and their ecological attraction to environmental disaster.” He knew he’d piqued my interest. “These little creatures have existed for over forty million years, Lynna. Without sex! And they’re everywhere. In temporary ponds, moss, even tree bark. Bdelloid mothers that go through desiccation produce daughters with increased fitness and longevity. In fact, if desiccation doesn’t occur over several generations, the rotifers lose their fitness. They need the unpredictable environment to keep robust.” They incorporate genes from their environment: they acquire DNA transposons—mobile DNA—through HGT.”

—A DIARY IN THE AGE OF WATER

The bdelloid all-female populations have thrived for millions of years by maintaining a robust and diverse population through epigenetics and DNA repair during dormancy…The dormancy of all-female bdelloids is an elegant technique to ride out harsh conditions. The bdelloids can go dormant quickly in any stage of their life cycle, and they’re capable of remaining dormant for decades. They can recover from their dormancy state within hours when the right conditions return and go on reproducing without the need to find a mate.

Highly variable environments tend to support rare species: organisms that are uniquely equipped for change. These are the explorers, misfits, and revolutionaries who do their work to usher in a new paradigm. They carry change inside them, through phenotypic plasticity, physiological stress response mechanisms, or life history adaptations. Like bdelloid rotifers going dormant through anhydrobiosis. Or blue-green algae forming dormant akinete spores. In tune with the vacillations of Nature, epigenetics-induced adaptation is the only option for keeping up with rapid and catastrophic environmental change, not to mention something as gigantic as climate change. That’s why the bdelloid rotifers survived for millennia and will continue for many more. They adapt by counting on change.

Maple swamp forest in Trent Nature Sanctuary, ON (photo and rendition by Nina Munteanu)

References:

Munteanu, Nina. 2020. “A Diary in the Age of Water.” Inanna Publications, Toronto. 300pp.

Munteanu, Nina. 2016. “Water Is…The Meaning of Water.” Pixl Press, Vancouver. 586pp.

O’Leary, Denise. 2015. “Horizontal gene transfer: Sorry, Darwin, it’s not your evolution anymore.” Evolution News, August 13, 2015. Online: https://www.evolutionnews.org/201508/horizontal_gene/

Ricci, C. And D. Fontaneto. 2017. “The importance of being a bdelloid: Ecological and evolutionary consequences of dormancy.” Italian Journal ofZoology, 76:3, 240-249.

Robinson, Kelly and Julie Dunning. 2016. “Bacteria and humans have been swapping DNA for millennia”. The Scientist Magazine, October 1, 2016. Online: https://www.the-scientist.com/?articles.view/articleNo/47125/title/Bacteria-and-Humans-Have-Been-Swapping-DNA-for-Millennia/

Weinhold, Bob. 2006. “Epigenetics: the science of change.” Environmental Health Perspectives, 114(3): A160-A167.

Williams, Sarah. 2015. “Humans may harbour more than 100 genes from other organisms”. Science, March 12, 2015. Online: http://www.sciencemag.org/news/2015/03/humans-may-harbor-more-100-genes-other-organisms

Nina Munteanu is a Canadian ecologist / limnologist and novelist. She is co-editor of Europa SF and currently teaches writing courses at George Brown College and the University of Toronto. Visit www.ninamunteanu.ca for the latest on her books. Nina’s bilingual “La natura dell’acqua / The Way of Water” was published by Mincione Edizioni in Rome. Her non-fiction book “Water Is…” by Pixl Press (Vancouver) was selected by Margaret Atwood in the New York Times ‘Year in Reading’ and was chosen as the 2017 Summer Read by Water Canada. Her novel “A Diary in the Age of Water” was released by Inanna Publications (Toronto) in June 2020.

The Invasion of Giant Crayfish Clones & A Diary in the Age of Water

OLYMPUS DIGITAL CAMERA

Marmorkrebs, giant marbled crayfish

In 2018, scientists reported that the giant marbled crayfish (Marmorkrebs [German]: Procambarus fallax f. virginalis) recently developed the strategy of being entirely female and cloning itself via parthenogenesis1; the female doesn’t require a male crayfish to fertilize its eggs. Despite the cloning procedure that makes them virtually identical genetically, the crayfish vary in size and pattern—no doubt due to epigenetics.2

First discovered by a German aquarium in the mid-1990s, these crayfish that developed from Florida-Native crayfish have migrated into the wild and are aggressively spreading in Europe, at the expense of the native European crayfish. The 8 to 12 cm long Marmorkrebs has been observed in Germany, Italy, Slovakia, Sweden, Japan, and Madagascar. The marbled crayfish prefers a warm and humid climate, suggesting that climate change may influence its distribution and success. The clones also thrive in a wide range of habitats—from abandoned coal fields in Germany to rice paddies in Madagascar, writes Carl Zimmer of the New York Times.

Given that every individual Marmorkrebs can reproduce (the advantage of parthenogenesis is that the female crayfish doesn’t need to find a mate—it just gives birth), one European scientist has dramatically suggested that, “we’re being invaded by an army of clones.” Zimmer shares the results of Dr Lyko and his team on how the all-female Marbokrebs came to be:

“Scientists concluded that the new species got its start when two slough crayfish mated. One of them had a mutation in a sex cell — whether it was an egg or sperm, the scientists can’t tell. Normal sex cells contain a single copy of each chromosome. But the mutant crayfish sex cell had two. Somehow the two sex cells fused and produced a female crayfish embryo with three copies of each chromosome instead of the normal two. Somehow, too, the new crayfish didn’t suffer any deformities as a result of all that extra DNA.” 

In its first couple decades, [Marmorkrebs] is doing extremely well, writes Zimmer. But sooner or later, the marbled crayfish’s fortunes may well turn, he adds. “Maybe they just survive for 100,000 years,” Dr. Lyko speculated. “That would be a long time for me personally, but in evolution it would just be a blip on the radar.”

marbled-crayfish2

Marmorkrebs

But what if this speculation isn’t the whole scenario? What if Marmorkrebs is just another example of climate change-induced adaptation and change through epigenetics? While climate forcing and habitat destruction is causing the extinction of many species; other species are, no doubt, adapting and exploiting the change. These generalists (born with change inside them) are poised to take over in Nature’s successional march.3

Bdelloid-rotifer-Philodina-gregaria

Bdelloid rotifer

Parthenogenesis and epigenetic change isn’t new. In fact, it’s very old … All-female bdelloid rotifers have been cloning a sisterhood for millions of years and using incorporated foreign genes through horizontal gene transfer4 (essentially stealing genetic material from their environment) to maintain a healthy diverse population. What’s new and weird is that this crayfish “suddenly” developed this ability—probably through epigenetic means (given this entire group is versatile in reproductive strategies in general). The real question none of the articles that covered this phenonemon ask is: WHY? Why is it happening NOW?

In my latest book A Diary in the Age of Water (due for release in May 2020 by Inanna Publications) I explore this “change” in a unique way:

Diary Water cover finalKyo finds a copy of Robert Wetzel’s Limnology on a lower shelf of the “L” section. It stands tall with a thick green-coloured spine. This is the book that Hilda, one of the Water Twins, had saved from the book burnings of the Water Age. A present from her limnologist mother. Hilda kept it hidden under her mattress. When CanadaCorp police burst into their home and dragged her mother away, Hilda was left alone with Wetzel. The limnology textbook was forbidden reading because its facts were no longer facts. 

After some coaxing, Myo shared a most bizarre tale of that time which led to the catastrophic storms and flood. What the governments hadn’t told their citizens—but what each citizen felt and knew—was that humans had lost the ability to reproduce. Then a spate of “virgin births” throughout the world spawned what seemed a new race of girls—‘deformed’, blue and often with strange abilities. Many considered them abominations, a terrible sign of what was in store for humanity—a punishment for their evil ways. Then, as quickly as they’d populated the world, these strange blue girls all disappeared without a trace. They simply vanished and became the Disappeared. Myo told her that some people called it a Rapture, a portent of the end times. Others suggested that the girls had all been murdered—a genocide, organized by what was left of the world government. 

Then … the storms … changed the world.

–“A Diary in the Age of Water” 

  1. Spontaneous Parthenogenesis: From the Greek Parthenon “virgin” and genesis “creation”, parthenogenesis is a natural form of asexual reproduction in which growth and development of embryos occur without fertilization. In animals it involves development of an embryo from an unfertilized egg; in plants it proceeds through apomixis. The production of only female offspring by parthenogenesis (such as with bdelloid rotifers) is called thelytoky.
  2. Epigenetics is the study of changes in organisms caused by the modification of gene expression (such as environmental triggers) rather than alteration of the genetic code itself. If genetics represents the hardrive of a computer, epigenetics is its software.
  3. Niche (the role or job of an organism or population) can be broad (for generalists) or narrow (for specialists). A specialist has superior abilities to exploit the narrow environmental conditions it lives in and is splendidly adapted to a fixed stable environment; generalists, less successful at exploiting than the specialist but more widely adaptive, can thrive in less stable environments that present a wider range of conditions.
  4. Horizontal gene transfer is the movement of genetic material between organisms other than by the vertical transmission of DNA from parent to offspring through reproduction. HGT is an important factor in the evolution of many organisms.

A Diary in the Age of Water will be released in May 2020 by Inanna Publications, Toronto, Canada.

 

nina-2014aaa

Nina Munteanu is a Canadian ecologist / limnologist and novelist. She is co-editor of Europa SF and currently teaches writing courses at George Brown College and the University of Toronto. Visit www.ninamunteanu.ca for the latest on her books. Nina’s bilingual “La natura dell’acqua / The Way of Water” was published by Mincione Edizioni in Rome. Her non-fiction book “Water Is…” by Pixl Press (Vancouver) was selected by Margaret Atwood in the New York Times ‘Year in Reading’ and was chosen as the 2017 Summer Read by Water Canada. Her novel “A Diary in the Age of Waterwill be released by Inanna Publications (Toronto) in June 2020.