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Home / Archive / November 2022, Issue 1 / Features

Do Epigenetic Changes Influence

Evolution?
Evidence is mounting that epigenetic marks on DNA can
influence future generations in a variety of ways. But how
such phenomena might affect large-scale evolutionary
processes is hotly debated.

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Katarina Zimmer Share:

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T
he past few years have been a stressful time for
T
he past few years have been a stressful time for
ABOVE:
some of the hermaphroditic nematode worms © SCIENCE PHOTO
LIBRARY, JOSE
in geneticist Oded Rechavi’s lab at Tel Aviv ANTONIO PEÑAS
University in Israel. Raised at 25 degrees Celsius—a
sweltering temperature for C. elegans—the worms have resorted to an
unusual coping mechanism: early sex.

Hermaphrodites typically create

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offspring through self-
fertilization until three to four
days into adulthood, at which
point they start mating with
males. But Itai Toker, a former
PhD student in Rechavi’s lab, and
his colleagues noticed that when
the nematodes had been kept in
warm conditions for a few
generations, they would start to
exude male-attracting
pheromones just a day after
completing their larval
development and becoming an
adult. That appeared to give them
an advantage: When given the choice, male worms tended to mate with
these precocious worms more frequently than with ones raised under
normal temperatures.

The early sexual attractiveness may be a useful stress response, Rechavi tells
The Scientist. More mating means more mixing of different genomes,
boosting the progenies’ chances of securing a beneficial allele that will help
them weather the taxing environment, he explains. “When you mate, you
increase genetic variability” among your offspring.

Continuing to house the nematodes in warm temperatures, the team

observed that the premature attractiveness stuck with the worms for at least
a dozen generations. Even after the worms were moved back to cooler
conditions, the pheromone boost stuck around for three generations,
suggesting that the characteristic can be inherited—something Rechavi says
he found remarkable. Thanks to their ancestors’ experiences, worms that
had never experienced those torrid temperatures still matured earlier.
Around the fourth generation in cooler temps, however, worms lost this
trait, hinting that there’s a tradeoff to this early mating; sexual outcrossing is
generally costly to hermaphrodites as their overall genetic contribution to
the next generation is lower, says Toker, who’s now a postdoc at Columbia
University. The fact that the early maturation trait was lost also suggested it
had an epigenetic basis. Additional experiments showed that small RNAs
targeting genes that are involved in sperm development and function were
being passed from parent to offspring in the hermaphrodites’ gametes.
When the team blocked the transmission of small RNAs, the nematodes
didn’t pass on the trait.

“ The evidence from classical genetics, I should

say, is pretty strongly against this being
anything at all frequent.
—Brian Charlesworth, University of Edinburgh

Research from other groups has yielded similar evidence that there’s
sometimes more to heredity than DNA alone. In C. elegans, the small RNA
”
mechanisms have been shown to transmit acquired traits, including
starvation-induced adaptations to food scarcity and avoidance behaviors
that prevent the worms from ingesting pathogenic bacteria, even after the
initial trigger is gone. “Once it’s going, it seems to just keep going for some
time,” says epigeneticist Alyson Ashe of the University of Sydney. Besides
RNAs, epigenetic factors such as proteins and other molecules that interact
with the genome and direct which genes are expressed have also been found
to be passed from parent to offspring in several plant and animal species,
sometimes with consequences that affect the fitness of future generations.

Some evidence suggests that epigenetic changes have the potential to

influence a lineage’s genetics. Rechavi says that in his study, he’d expect that
the nematodes that experienced an earlier start to their mating activity
would see an increase in the genetic diversity of their offspring. “This is the
punchline of the paper: That a transient small RNA-based response can lead
to a permanent change in the genome,” he says. And across a range of
species, scientists have learned that extragenomic components can directly
change the genetic code by triggering mutations and shaping the evolution
of genes. Such revelations suggest that epigenetics could be a long-
overlooked player in evolutionary processes, sparking new hypotheses about
how species adapt and diversify.
Still, much of the scientific community has expressed doubt that such
mechanisms play significant roles in the long-term evolution of populations
and species. In many species, eggs and sperm undergo epigenetic
“reprogramming,” in which their genomes are largely scrubbed clean of
certain epigenetic changes. The uncertainty around the scale and
evolutionary importance of epigenetic phenomena is fueling fierce debate
about what such findings mean for the foundational evolutionary theories
that have shaped science for the better part of the past century. Specifically,
the Modern Synthesis developed in the 1940s supposes that evolution is
driven solely by random DNA mutations. While many scientists question
whether non-DNA-based mechanisms could be meaningful contributors to
evolutionary processes, some say that textbooks are due for an update.

“We don’t need to rewrite and throw away the current theories, but they’re
incomplete,” says Ashe. “They need adjustment to show how epigenetics can
interplay with those theories.”

Interpreting transgenerational epigenetic inheritance

The idea that epigenetic changes can be inherited across multiple

generations in animals only began to crystallize relatively recently, with the
first case in C. elegans reported in 2006, for instance. Examples of such
phenomena have been reported in mice, too, although some studies have
suggested that certain types of epigenetic inheritance might be rare in the
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rodents. Mammalian cells undergo two rounds of epigenetic reprogramming
during gamete production and early embryo development, removing the
majority of methylation marks from the DNA and reshaping the histone
modification landscape, explains molecular biologist Joan Barau of the
Institute of Molecular Biology in Mainz, Germany. He adds that in his view,
the evidence so far suggests that mammals lack RNA-dependent RNA
polymerases (RdRPs), the enzymes that propagate RNA signals across
multiple generations in C. elegans. The difficulty in deciphering the
mechanism of transmission of epigenetic marks has made it hard to
convince many researchers that such intergenerational processes can occur
in mammals, says Alexandra Weyrich of the German Centre for Integrative
Biodiversity Research Halle-Jena-Leipzig. “The main problem is that we
don’t know yet how [epigenetic changes are] transmitted to the next
generation. If we solve that, then [the idea of epigenetic inheritance in
mammals would be] more accepted [by] evolutionary biologists and
geneticists.”

The number of species in which transgenerational epigenetic inheritance

has been persuasively demonstrated remains small. Nevertheless, such
findings raise an important question, says evolutionary biologist Dragan
Stajic of the University of Bern in Switzerland. “If we know now that
epigenetic changes can produce variation, and they can be inherited . . . then
of course, the logical question is, can evolution act upon this?”
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To some scientists, the fact that cases of transgenerational epigenetic

inheritance are often ephemeral—typically lasting only a handful of
generations in C. elegans, for instance—argues against a significant
evolutionary role. For simple traits controlled by single genetic loci, it would
be hard for natural selection to produce a population where all individuals
bear the same beneficial phenotype if that trait were unstable and reversed
in some lineages, says Brian Charlesworth, an evolutionary geneticist at the
University of Edinburgh. “That’s one problem, I think, for believing that this
is an important evolutionary process—the apparent lack of stability in many
of these cases where it does seem to be well-documented,” Charlesworth
says.

That’s why some scientists see epigenetic inheritance as no more than an

adaptation in and of itself—perhaps a kind of bet-hedging strategy to
transiently adapt to short-term environmental stressors without committing
to stably transmitted, hard-wired changes. Stajic and colleagues recently
tested that idea in the budding yeast Saccharomyces cerevisiae. They
engineered yeast strains to have different expression patterns of the uracil
synthesis gene URA3 and cultured the fungi in environments that were
either changing or constant to see which strains would fare best. The team
created the strains by inserting URA3 into areas of the yeast genome known
to carry heritable epigenetic factors that cause genes to be either continually
expressed or switched on and off at a slow or fast rate. In a regular cell
growth medium, the nonswitchers quickly outnumbered the switchers.
However, in an experiment that alternated between normal media and one
that produces a toxic byproduct when metabolized by the URA3 enzyme—at
the same rate as the switchers’ changes in gene expression—the switching
strains surged to dominance within 20 generations. “Indeed, we do show
that epigenetic inheritance is more beneficial in the fluctuating
environments where the conditions change rapidly,” Stajic says. Such
mechanisms of adaptation could be of particular importance for species like
C. elegans, Ashe adds, which face challenges such as seasonal temperature
fluctuations that last only a few months, or a handful of worm lifetimes.
In some ways, whether this kind of transient change amounts to evolution of
a population is a semantic issue. Many scientists don’t consider such
epigenetically-driven adaptation as evolution, simply because it doesn’t
involve changes to coding sequences. “I guess I’m ‘old school’ and would still
fall back on the classic definition of evolution as including true genetic
change. . . . I’d have to think carefully about the alternate idea of epigenetic
‘evolution,’” says evolutionary geneticist Michael Goodisman of Georgia Tech
via email. But to others, such as evolutionary ecologist Christina Richards of
the University of South Florida, any kind of heritable change in trait
variation should be considered evolution. She points to one of her study
species, the invasive knotweed Reynoutria japonica, which has adapted to
diverse beach, roadside, and salt marsh habitats. Plants don’t appear to
undergo as much epigenetic reprogramming in the germline as animals do,
and seem to pass on many methylation patterns quite robustly. If knotweed
is acquiring and transmitting epigenetic traits that aid survival in new
habitats, she says, “it’s going to affect how well they do; it’s going to affect
how much offspring they have. That’s evolution.”

See “DNA Methylation Plays Important Roles in Plant Biology”

Richards adds that with DNA-based changes dominating evolutionary

theory for so long, it may well be an uphill battle to convince scientists that
theory for so long, it may well be an uphill battle to convince scientists that
other mechanisms contribute. “We’ve been steered by that opinion for a long
time,” she says. “If you define evolution as changing allele frequency over
time, then we have nowhere to start, and that’s the real problem. . . . I’m not
trying to say that it’s all epigenetic. I’m just trying to ask the question
[whether it’s involved].”

In fact, inherited epigenetic traits don’t necessarily need to be adaptive to

influence evolution, notes behavioral geneticist Benjamin Oldroyd of the
University of Sydney. The idea of organisms acquiring an adaptive trait
during their lifetime and transmitting it to their offspring—often described
as Lamarckian evolution—has long been considered controversial and such
phenomena have only been observed in organisms like C. elegans and
potentially in certain plants. All it takes for epigenetics to affect evolution,
Oldroyd says, is a change in gene expression—triggered, for instance, by an
environmental perturbation—and for those epigenetic marks to be
inherited. Moreover, Stajic adds, if some organisms habitually pass down
certain traits epigenetically, as do many plant species, then any random
errors that occur during the transmission of those marks could produce new
heritable epigenetic traits. In theory, natural selection could act on all these
types of epigenetic changes, Stajic says.

Some researchers note that the evidence for transgenerational epigenetic

inheritance—and especially its role in evolutionary processes—outside of
laboratory organisms remains thin. In plants, for instance, which have been
eagerly studied for such effects, “The most we can say is that we have clues
that epigenetic mechanisms might have a role in adaptation,” says plant
ecologist Teresa Boquete of the Universidade de Santiago de Compostela in
Spain. Many studies in wild plant species have been limited to describing
broad epigenetic differences across individuals, and it’s often unclear
whether these changes have taken place within an organism’s lifetime or if
they’ve been inherited across generations, she says. Another challenge with
they’ve been inherited across generations, she says. Another challenge with
wild populations that aren’t genetically identical is that the observed
patterns may not be purely epigenetic, if there are underlying mutations in
the genes encoding the organism’s epigenetic machinery, Richards notes.
“Even one change in DNA sequence can dramatically change the
methylation patterns in the genome.”

In humans, the evidence is even harder to interpret, with correlational

studies so far failing to yield definitive answers about transgenerational
epigenetic inheritance, Barau says. “I’m not a total [skeptic] of
transgenerational epigenetic inheritance, it’s just that the burden of proof
for this is quite high. And it hasn’t been achieved in many of the [claims],
especially when you’re talking [about] humans.”

See “Does Human Epigenetic Inheritance Deserve a Closer

Look?”

Epigenetics and the Genome

Scientists are learning that epigenetic marks such as DNA methylation

can influence not just gene expression, but genes themselves. When this
happens in germline cells, the changes can diversify the genetic
substrate upon which natural selection acts. Scientists are still exploring
how such processes could influence evolutionary processes overall.

Triggering mutations
Scientists have known for several decades that methylation can cause
the nucleobase cytosine to lose an amino group, transforming it into
thymine. When this occurs during gametogenesis, it can be one of the
major drivers of evolution at the molecular scale. Some human embryo
studies estimate that for particular genomic regions, some 20 percent of
mutations unique to humans arose from cytosine methylation.

Shaping mutation patterns

Some studies in cancer cells suggest that the packaging of DNA into
dense structures called nucleosomes not only shapes the expression of
those genes, but also their mutation rates. When bound in such
conformations, DNA is less likely to open into a single-stranded state
that makes it more prone to mutations.

Dampening mutation

Epigenetic dynamics can also slow evolutionary processes by

suppressing transposable elements, snippets of DNA that hop around
the genome and cause mutations. Genes neighboring these
troublemakers can end up being silenced too, sometimes creating a
conflict between the need to express genes and the need to silence
transposons. In certain Drosophila species, researchers hypothesize that
the flies have moved large chunks of the transposon-infested Y
chromosome to other chromosomes to ensure important genes are not
silenced.

New gene functions

 New gene functions

Long-term epigenetic silencing of particular genes could allow them to

accumulate genetic mutations and develop new functions over time.
There is some correlational evidence that duplicated genes—which are
often lost from the genome unless they are beneficial to the organism—
frequently become epigenetically silenced. They could thereby evolve
new functions.

THE SCIENTIST STAFF; © ISTOCK.COM, RUJIRAT BOONYONG; BASED ON CONCEPTS

REVIEWED IN S.V. YI, M.A.D. GOODISMAN, PHILOS TRANS R SOC LOND, B, BIOL SCI,
376:20200114, 2021.
See full infographic: WEB | PDF

Effects of epigenetics on the genome

Given the often short-lived nature of epigenetic inheritance, one way that
inherited extra-genomic factors could influence evolution is by changing the
DNA itself—a phenomenon for which there is some evidence now
surfacing. (See illustration.) Rechavi’s group has shown this can occur for an
animal, albeit indirectly, by promoting sexual reproduction in the worms
and thereby turbocharging their genetic evolution. In that case, the
mutations that make their way into young worms’ DNA through genetic
recombination are random and scattered across the genome; the effect of
recombination are random and scattered across the genome; the effect of
the epigenetically inherited trait is simply that their general genetic diversity
is increased—although Rechavi adds that the team didn’t sequence the
offspring’s genomes to explore how exactly this ultimately affects genetic
evolution.

Another hypothesis that some scientists have floated in the literature is that
inherited epigenetic regulation of particular genes can influence genetic
adaptation at those specific genes. If an environmental pressure maintains
long-term gene silencing, for example, the gene could naturally accumulate
random mutations over time, changing its function or, more likely,
rendering it defunct. At some point, “that epigenetic silencing of that gene
would no longer be required because the gene has mutated anyway,” Ashe
says.

That idea hasn’t yet been tested in animals, Ashe cautions. But a 2019 study
by Stajic and colleagues provides some proof of concept in yeast cells that
had been engineered to have URA3 partly silenced. When the researchers
placed the strains in a potentially toxic growth medium, “We actually see
that this first step in adaptation is through epigenetics,” Stajic says.
Specifically, the cells strengthened silencing of URA3, and some generations
later, knockout mutations popped up that rendered the gene defunct. In this
way, epigenetic inheritance could form a kind of bridging mechanism to
long-term change, Stajic says—in essence, a “soft” adaptation to probe the
waters, followed by a hard-wired change that will stick in the genome
indefinitely. “It seems that epigenetics, in this case, acts as a buffering
system that allows the population to survive this initial step . . . until the
beneficial mutation appears and fixes,” he says.

“ We don’t need to rewrite and throw away the

“ We don’t need to rewrite and throw away the
current theories, but they’re incomplete.
—Alyson Ashe, University of Sydney

More directly still, some epigenetic marks have long been known to induce
mutations and shape mutational patterns across the genome. Methylation
”
marks, for instance, are known to trigger a chemical reaction that mutates
cytosine into a different base, thymine. Methylation patterns also influence
genomic stability by repressing highly mutagenic DNA snippets called
transposable elements. “These stability changes can influence the DNA
sequence directly, which subsequently can lead to genetic adaptation,”
Weyrich says. A recent analysis of the Arabidopsis thaliana genome suggests
that mutations aren’t truly random but are shaped by epigenetic marks,
including not just methyl groups but also histone modifications and the
general accessibility of chromatin. When such mutations occur in germline
cells and become inherited across generations, they have the potential to
influence a species’ evolution, Goodisman says.

Through mechanisms like these, says evolutionary biologist and philosopher

of biology Eva Jablonka of Tel Aviv University, epigenetic inheritance could
even lead to the diversification of species. “The first thing that happens in an
environment is an adaptation at the physiological level,” she says, “and then
anything that helps [the organism] to get stabilized will be selected.” So far,
there is only correlative support for this idea. She points to research in
darter fish (genus Etheostoma) suggesting that methylome differences are
greater than genetic differences between two closely related but physically
separated fish populations; the authors hypothesize that epigenetic
differences could be driving reproductive isolation between them. Similar
observations have been made in populations of the spiny mouse Acomys
cahirinus and in farmed breeds of the European sea bass Dicentrarchus
labrax. In the sea bass, researchers even found that epigenetic differences
identified in early domesticated populations overlapped with cytosine-to-
thymine mutations documented in samples that had undergone 25 years of
selective breeding. And, the fact that phenotypic diversity between species is
greater than can seemingly be explained by genome differences alone—with
just a few percent sequence difference between chimpanzees and humans,
for instance—hints that factors other than DNA play a role in species
diversification, Weyrich adds. “If we exclude this flexible mechanism
completely . . . then you just miss a very important piece of evolution and of
diversity.”

The role of epigenetics in speciation is still debated. “I’m not saying there
isn’t something there, but . . . solid evidence is really lacking,” says
Charlesworth. That’s perhaps because such evidence is simply hard to get, he
notes. It’s difficult to robustly quantify epigenetic changes between
populations, because epigenetic patterns vary so much between individuals
and even within an individual’s lifetime. Compared to genetic mutations,
which can be quantified with reasonable accuracy, “when it’s something like
the amount of methylation, it’s a much vaguer sort of statistic.”

A future full of questions

While many questions surrounding epigenetic inheritance remain unsettled,

Jablonka sees the evidence accumulated thus far as a validation of
hypotheses she and others conceived of decades ago. She and evolutionary
biologist Marion Lamb saw the potential of epigenetics to influence
evolutionary processes in the 1980s after separately studying epigenetic
processes in cells of different rodent species and fruit flies. The pair
conceptualized epigenetic inheritance as another evolutionary driver,
alongside genetic change and the behavioral and cultural transmission of
traits. All four pathways can generate heritable variation on which natural
selection acts, they wrote in their 2005 book, Evolution in Four
selection acts, they wrote in their 2005 book, Evolution in Four
Dimensions.

These notions are key to the Extended Evolutionary Synthesis (EES), a

theoretical framework that aspires to be a complement to the DNA-centered
views laid out in the Modern Synthesis. In the EES view, evolution occurs
not solely by changes in genetic allele frequency, but via any kind of
heritable variation in traits—a view that Jablonka sees as increasingly
supported. “The more people look, the more they find.”

Charlesworth, however, doesn’t see epigenetic inheritance as a challenge to

fundamental rules of evolution laid out in the Modern Synthesis. Many
documented cases involve subtle traits pertaining to stress responses and
fertility, and not lineage-defining evolutionary innovations such as eyes or
wings, for instance. In his view, it’s likely that the documented cases of
epigenetic inheritance in worms, plants, and mammals are exceptions to the
normal rules of heredity, he says. “The evidence from classical genetics, I
should say, is pretty strongly against this being anything at all frequent.
People have been working on genetics for over 120 years. There’s a huge
body of evidence on . . . how [traits are] inherited.”

Such discussions tap into a broader argument that has long raged over the
EES, with frustration on both sides, researchers tell The Scientist. A recent
article in The Guardian titled “Do we need a new theory of evolution?”
generated rigorous debate among scientists on Twitter. “This all brings very
heated discussions [at] the conferences and meetings,” Stajic says via email.
“It is definitely very exciting times to be in the field.”

The outcome of this rift—as least as far as the evolutionary role of

epigenetics is concerned—hinges in part on the continued hunt for such
phenomena. To that end, Stajic is planning a study on stress adaptation in
zebrafish, while Richards says she’ll continue to probe knotweed for
epigenetic effects. Rechavi, meanwhile, hopes someday to scrutinize wild
isolates of C. elegans or of other worm species to see if they behave anything
like their laboratory counterparts. He finds it hard to believe that the
observations made so far are just a coincidence. “My feeling is that it’s quite
unlikely that we happen to find it in just [a few] of the . . . model organisms
of biology and it doesn’t exist in any other organism,” he says. “This seems
like too much luck.”

THIS EXCLUSIVE ARTICLE WAS FIRST PUBLISHED IN TS DIGEST

This Issue
November 2022, Issue 1

Epigenetics in
Evolution
Researchers debate the influence of
extragenomic processes on
evolutionary change

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Keywords

DNA methylation, epigenetic, epigenetic regulation, epigenetic regulators,

epigenetics, epigenome, epigenomics, evolution, evolutionary biology, genetics,
lncRNA, long noncoding RNA, methylation, microRNA, microRNAs, mutation,
mutations, natural selection, RNA, RNA epigenetics, transfer RNA,
 transgenerational epigenetic inheritance

Meet the Author

Katarina Zimmer

After a year teaching an algorithm to differentiate between the

echolocation calls of different bat species, Katarina decided she was
simply too greedy to focus on one field. Following an internship with
The Scientist in 2017, she has been happily freelancing for a number
of publications, covering everything from climate change to
oncology.

View full profile.

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