Bdelloid rotifers - 80 million years without sex

This article is reposted from the old Wordpress incarnation of Not Exactly Rocket Science. The blog is on holiday until the start of October, when I'll return with fresh material.

Sex is, on the whole, a good thing. I know it, you know it, and natural selection knows it. But try telling it to bdelloid rotifers. These small invertebrates have survived without sex for some 80 million years.

Bdelloid rotifers under the microscopeWhile many animals, from aphids to Komodo dragons, can reproduce asexually from time to time, it's incredibly rare to find a group that have abandoned sex altogether. The bdelloid rotifers (pronounced with a silent b) are an exception.

They live in an all-female world and since their discovery, not a single male has ever been found. Genetic studies have confirmed that they are permanently asexual, and females reproduce by spawning clone daughters that are genetically identical to them.

The bdelloids pose a problem for evolutionary biologists, who have struggled to explain how they could make do without a strategy that serves the rest of the animal kingdom very well. Now, Natalia Pouchkina-Stantcheva, Alan Tunnacliffe and colleagues from the University of Cambridge have found out how they do it.

Sexual animals have two copies of each gene that have only minimal differences between them. But the asexual bdelloid lifestyle has uncoupled the fates of each copy in a gene pair, allowing them to evolve in new directions. They get two genes for the price of one.

One of the vaunted benefits of sex is that it acts as a crucible for genetic diversity. Animals receive one pair of every gene from their mother and one from their father. As the pairs are united in the embryo, they are often shuffled into new combinations.

This genetic mingling can unite beneficial mutations in individuals who reap extra benefits. It can also unite harmful mutations in individuals that perform poorly in nature's trials and are weeded out. In this way, sex speeds up the spread of both beneficial mutations and the disappearance of harmful ones.

Asexual reproduction carries none of these benefits and some scientists see it as a poor and plodding long-term strategy that leaves a species unable to quickly adapt to new challenges. But the bdelloids are proof that permanent asexuality works and they have a way of creating genetic diversity that is all their own.

The genetic shuffling that accompanies sex means that even though an individual has two copies of every gene, they are mostly the same. Small differences between the two copies can have significant effects, but they are small differences nonetheless. For example, in other rotifer groups that still practice sex, an individual's gene pairs are at least 97.6% identical to each other.

But in the asexual bdelloids, a daughter inherits both copies of each gene from its mother and they never mingle. This frees them to evolve in their own directions and take on new roles, irrespective of the destinies of their partner.

Pouchkina-Stantcheva found evidence of this in a gene called lea from the bdelloid Adineta ricciae. The two copies of this gene differ by about 14% of their sequence, and these small differences translate to proteins with substantially different structures and functions.

Bdelloids live in freshwater pools but can survive periods of drought by dehydrating and living in a dry and dormant state. Both LEA proteins protect the animal in this state, but they do so in complementary ways.

Version A acts as a molecular shield and prevents more sensitive proteins from balling together into useless clumps when they dry out. Its partner, version B, insinutates itself into the fatty membranes that surround all cells and helps to stabilise them.

By sending two copies of a single gene down different evolutionary paths, natural selection has provided A.ricciae with two separate ways of protecting itself from drought. The researchers believe that this two-for-the-price-of-one deal on protein diversity helps to compensate for the loss of diversity that accompanies a shunning of sex.

Many major evolutionary steps have occurred through a remarkably similar process called 'gene duplication'. During the genetic shuffle that accompanies sex, a gene is mistakenly duplicated an the extra redundant copy is free to evolve new functions.

The bdelloids use essentially the same process but they don't need to create another copy of their genes when they already have two independent copies. It's a strategy that doesn't seem to have held them back - about 400 different species of bdelloid rotifers swim in today's ponds.

More on rotifers:

Reference: Pouchkina-Stantcheva, McGee, Boschetti, Tolleter, Chakrabortee, Popova, Meersman, Macherel, Hincha & Tunnacliffe. 2007. Functional divergence of former alleles in an ancient asexual invertebrate. Science 318: 268-271.

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Why all females and not all males? If there's just one gender, how do one tell if it's male or female?

The short answer Carlos, is that the single gender produces the eggs and therefore is female!

There are approximately 360 species of bdelloid rotifers occupying the Class Bdelloidea with no known males in any of the species... the reproductive processes take place in the trunk which contains "germovitellaria"- these are the gonads that produce the eggs ("germarium") and the yolk ("vitellaria")- the eggs produced are largish and oval in shape with some species of rotifer having two germovitellaria and some only having one.

I believe, and please correct me if I am wrong, that the basic 'template' is female, at least in humans. It's the effect of hormones during pregnancy that turns some foetuses into males. In which case, perhaps these are all females because that's the default? Or simply because they're having, for want of a better word, offspring?

By archaeozoo (not verified) on 30 Sep 2009 #permalink

re. comment #3... EGGS!

LOL! I believe Ernst Mayr's answer to the "species problem" is to define species as "groups of actually or potentially interbreeding natural populations, which are reproductively isolated from other such groups" which stresses reproduction as opposed to gender- rotifers obviously reproduce... however the common accepted interpretation of species is "populations of organisms that have a high level of genetic similarity" but I would agree that in microbiology there is a clear argument for the entire bacterial domain being a single gene pool which would probably support the contention of many entomologists who would argue that most, if not all mammal "species" should really be classified into one genus!

Is science supposed to be an exact science?

How is it that they can maintain their identities as species? Wouldn't the genome of separate family trees of individuals slowly and amorphously diverge, resulting in a broad class of organisms with less commonality as time goes on? Do they converge on similar solutions to environmental challenges?

Mark,

Genetic diversity is maintained through the mechanism as outlined in Ed's article above: "but in the asexual bdelloids, a daughter inherits both copies of each gene from its mother and they never mingle. This frees them to evolve in their own directions and take on new roles, irrespective of the destinies of their partner."

Further, "Pouchkina-Stantcheva found evidence of this in a gene called lea from the bdelloid Adineta ricciae. The two copies of this gene differ by about 14% of their sequence, and these small differences translate to proteins with substantially different structures and functions."

What this means is that there is at least as much genetic differentiation as would exist between sexually-reproducing humans and as also stated above, those small variations can account for substantial differences (unless you have an identical twin, look at your own siblings, or even the next door neighbors! [and "monkey business" inferred from that is purely coincidental!])

Your argument would probably hold more true for other species that clone exact copies of mom through parthenogenesis (called "obligate parthenogenesis" if only females are produced) and therefore do not have the ability to keep the mom's and offspring's genes separate as rotifers do, then they would indeed be very prone to react negatively to sudden changes in their environment.

Mark: bdelloids haven't maintained their identity as a single species, instead they've differentiated into a variety of species.

The concept of species is somewhat theoretical under normal circumstances but for these ladies it's even more theoretical, merely describing groups of similar individuals that were related in the past but (obviously) don't interbreed. Similar objections are made to describing bacteria as species, although bacteria at least have a few mechanisms for lateral gene flow.

I'm curious why the gene differentiation trick works for bdelloids and not for other multicelluar animals. I'm guessing that others undergo meiosis and then recombine the genes internally, mimicking sex, while bdelloids skip that step entirely.

@John S. Wilkins,
The Biological Species Concept (BSC) is just one of many. In the paper: Concepts of Species by James Mallet (2001). He attempts to discuss all of the current concepts and their implications with regard to evolutionary and conservation sciences. It is a great paper with a concise description of species concepts.

I am a fan of the Phylogenetic Species Concept (PSC) over the BSC because it is much more precise: " A phylogenetic species is an irreducible (basal) cluster of organisms, diagnosably distinct from other such clusters, and wthin which there is a parental pattern of ancestry and descent"(Carcraft, 1989, Speciation and its ontology: The empirical concequences of alternative species concepts for understanding patters and processes of differentiation).

The PSC has its own disadvantages, namely it could be used to parse smaller and smaller groups until we classify individuals as species unto themselves. But I think with a reasonable adherence we stand the best shot of perceiving monophyletic groups using this method. Which in the long run will be more useful I think. Not that my opinion means much. hehe.

Anyway, the question of what exactly constitutes a species remains unsettled. There are many ideas, and many adhere to the BSC because of its historical popularity (and lets face it, Ernst Mayr was an amazing scientist)though I'm guessing the BSC won't be the definitive concept used to express the idea of discrete groups we call species.

DJ translated~

Biological Species Concept (BSC): reproductive isolation is the centerpiece, i.e. the failure of populations to interbreed or to form viable or fertile hybrids (insert Ernst Mayr here)

Phylogenetic Species Concept (PSC): monophyly is the centerpiece, i.e. the populations of each species should share a common ancestor (insert DJ here)

then we also have-

Ecological Species Concept (ESC) which defines a species as a set of organisms exploiting a single niche (adaptive zone), i.e. it supposes that ecological niches in nature occupy discrete zones (kinda almost insert me here!)

Well, Mayr was wrong, and probably didn't take bdelloids into consideration when he came up with his definition. Furthermore, many other species that were supposedly asexual were found to have males. However, there should be genomic "footprints" if sexual reproduction occured, and as Meselson and co. have shown, these are absent in bdelloids. These gals are the real deal when it comes to asexuality. And if you ever look at the different species under a microscope, some are so different in appearance, morphology, behavior, etc, that there is no doubt that they can be classified as separate species.

So , BEFORE 80 million years ago??? What prodded the evolution away from sexual reproduction to female cloning?
Too many orgies?

By alexandra (not verified) on 29 Jan 2010 #permalink