Imagine a
lineage made up solely of women. Generation after generation, these females
pilfer genes from
males—not mating and reproducing in the usual way, but using sex as a means to collect genetic
material that they can parcel out to their offspring in seemingly any
configuration. A few genes here, a few genes there, generation after
generation. It's not some Themyscira-esque
fantasy: some lady salamanders have been carrying on this way for
millions of years.
The
strange reproductive behaviors of the genus Ambystoma aren't new to science.
Researchers have known for some time that one lineage of these animals—a line
of salamanders that
only ever have female offspring—persist by collecting the genetic material of
males from several other species in the genus. But in case this is your first
time encountering the fantastical world of "kleptogenesis" (side
note: great word), here's a run-down.
Many
members of the salamander genus Ambystoma are sexual creatures—by which we mean
males drop sperm packets to fertilize female eggs, producing offspring with a
set of genetic instructions from each of their two parents. But unisexual
Ambystoma lizards do it better. These females pick up those packets, but they
can gather more than one with which to fertilize their eggs. And once they do,
it seems to be up to them to decide which parts of the genome—if
any—they use from each of their mates.
"Most
vertebrates that reproduce in ways that involve only females end up being
sperm-dependent in one way or another," says Maurine Neiman, associate
professor in biology at the University of Iowa. Many of those lineages become
"sperm parasites", requiring sperm to penetrate their eggs in order
to trigger development into embryos. They need that sperm to get
things going, but they throw the genetic material away—essentially creating
clone daughters while obeying the reproductive mechanics developed by their
sexually reproducing ancestors.
"Superficially,
these salamanders seem to have a lot in common with those other females,"
Neiman says. But in fact, their "bizarre" method of reproduction has
never been documented in another animal. And it's kept them alive for much
longer than other methods of makeshift asexual reproduction.
"They
have the same dependence on sperm, but they also keep the genomes—or some of
them, anyway—of the males they mate with," she explains.
The
female salamanders seem to be able to dole out genes to their daughters in all
sorts of configurations. Individuals are basically salamander hybrids made up
of the DNA of a variety of species, unified by common mitochondrial DNA (which a
mother passes directly to her children, with no male input) from an ancient
ancestor. Some carry five unique genomes around in the nuclei of their cells.
They appear to always carry at least one copy of the A. laterale genome (the
blue-spotted salamander), even though this species doesn't seem to be the one
from which they all descend. Scientists still don't know how a salamander
"chooses" what genes to give her daughter, but they know that mom can
basically make whatever kind of Franken-mander she desires.
"Let’s
say she’s got three copies of a genome," Neiman explains—plus one she was
born with. "She might not incorporate any of the surplus genes [into her
babies]. She might incorporate one of their genomes along with her own. She
might give them all three plus her own, so her baby has four. Or she could even
leave out the one she was born with and pass along the other three.”
"In
biology, one way to get at a question is to look at something weird."
In a
study published recently in Genome Biology and Evolution, Neiman and her
colleagues at the University of Iowa and The Ohio State University—led by a
graduate student from each lab—tried to puzzle out what the heck a salamander
does when spoiled for gene choice. And they were fueled by more than just
herpetological curiosity.
"We're
interested in the broader question of why genomes are organized as they are in
most animals," she says. "We typically have two copies. Why is that?
We don't have a good understanding of that. And in biology, one way to get at a
question is to look at something weird. You can sometimes understand the
typical by figuring out how the exception to the rule works.”
The
little lady her team studied was definitely an exception to the rule: she
carried three genomes, making her a "triploid" organism. Analysis of
her DNA revealed that most of the genes taken from males of other
species—Ambystoma laterale, Ambystoma texanum, and Ambystoma tigrinum—had been
expressed equally. Genes make us who we are by instructing our cells to make
certain proteins at certain times, contributing to specific bodily structures
and processes. We say a gene is "expressed" when it's allowed to do
the thing it's meant to do, leading to some physical result. If you've got
multiple genomes kicking around, you probably have genes that don't need to be
turned on—they might be duplicates of a gene from another source, or even
produce proteins that conflict with those made by different genes. According to
the new study, while a salamander seems to pass her ill-begotten genes down in
all manner of assorted mixtures, her daughter is likely to use the resulting
genomes pretty equally to dictate her bodily functions. That's unusual in the
world of hybrids.
"That
surprised us," Neiman says. "When you have hybrids, you usually think
one genome is going to be used preferentially while the other is shut down. But
these questions are typically asked in the context of plant hybrids." Many
of the crops we grow today have been hybridized so much throughout their
evolutionary history that they now carry many genomes; wheat has
six copies of each of its seven chromosomes. Scientists know an awful
lot more about plant hybrids than
strange critters like these salamanders, Neiman says, but it's possible that a
better understanding of how the extreme gene swapping works could help us breed
better crops in the future.
"You
start to wonder if this ability to have so much genomic flexibility set them up
to be able to use their bizarre method of reproduction," she says.
"Does this mean that in general, animals are more flexible about genome
use than plants?" Answering that question could help us understand more
about how the two kingdoms evolved.
It could
be that this balance is key to keeping the (kind of absurd) method of
procreation going. “If you have a team that’s unbalanced and loses a top
player, you won’t win,” Kyle McElroy, a graduate student in Neiman’s lab and
the paper’s corresponding author, said in a
statement. “But if every player is equal, then you don’t lose as much.”
Neiman
and her colleagues can't be sure whether the genome equality persists as things
get more crowded. The follow-up study that's "just crying out to be
done," Neiman says, would be to examine a salamander with even more
genomes—some females are born carrying a genome from five different species of
Ambystoma. More study is definitely needed to suss out these strange
salamanders.
The
promiscuity of Ambystoma can be hard to wrap your head around if you think
of species in the way most of us learn about them in school: individuals
that can reproduce with one another. Hybrids like the unisexual members of
Ambystoma muck that all up: they actually need to mate with multiple species in
order to avoid extinction. And far from being sterile mules, their daughters
continue to exhibit the incredible ability to steal and reconfigure genes for
generation after generation. But Neiman says that the creatures are just one
example of how fluid biology truly is.
"You’re
talking to an evolutionary biologist who thinks a lot of the talk about
speciation is just hype," she says. "We’re humans, we like to put
things in categories. But I’m not crazy about the idea that species are
concrete in biology, outside of human context. Defining a species is useful in
terms of research, but I'd say these salamanders demonstrate the messiness of
biology and evolution—the fascinating and complicated reality that remains when
you take the human need to put things into neat categories out of the
picture."
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