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Globalization, climate change, and

transgenerational epigenetic inheritance: will our

descendants be at risk?

Carlos Guerrero-Bosagna *and Per Jensen

Abstract

Transgenerational epigenetic inherit ance has gained increased attention d ue to the possibility that exposure to

environmental contaminants induce diseases that propaga te across generations through epigenomic alterations in

gametes. In laboratory animals, exposure to environmental tox icants such as fungicides, pesticides, or plastic compounds

has been shown to produce abnormal reproductive or metabolic phenotypes that are transgenerationally transmitted.

Human exposures to environmental toxicants have increased d ue to industrialization and gl obalization, as well as the

incidence of diseases shown to be transgenerationally transmitted in animal models. This new knowledge poses an

urgent call to study transgenerational consequences of current human exposures to environmental toxicants.

Keywords: Transgenerational epigenetic inheritance, Environmental exposures, Non-infectious diseases, Globalization,

Industrialization, Food industry

Transgenerational epigenetic inheritance

Transgenerational epigenetic inheritance has gained in-

creased attention due to the possibility that exposure to

environmental toxicants or other stressors can induce

long-lasting changes in lineages of organisms [1-3]. The

process involves germ line epigenomic changes that are

transmitted to future generations and that associate with

disease phenotypes [2,3]. Exposures to environmental tox-

icants such as fungicides, pesticides, or plastic compounds

have been shown in animal models to produce abnormal

reproductive or metabolic phenotypes that are transgener-

ationally transmitted. These include transgenerational in-

creases in the incidence of obesity, polycystic ovary

syndrome (PCOS), pregnancy defects, or germ cell apop-

tosis [4-8]. Importantly, the increased incidence of these

transgenerationally transmitted diseases in response to en-

vironmental exposures in animal models is sometimes

drastic. The current evidence on transgenerational epigen-

etic inheritance observed in animal models allows predict-

ing that environmental exposures of today ’s inhabitants of

the world will strongly impact the incidence of non-

infectious diseases in future generations. This would be

correlated with long-lasting alterations in the epigenome

of the gametes.

Current human exposures

Human exposures to environmental toxicants have

increased due to industrialization and globalization. The

current state of globalization and climate change have

helped the dispersion of toxicants in the environment by

increasing the global transport of pollution, mobilization of

legacy contaminants, and change in agricultural practices

[9,10]. As result, it is expected that the amount and time

that humans are exposed to en vironmental contaminants

will increase even further, with unpredictable health

consequences [9,10]. Moreove r, increasing production and

environmental accumulation o f new compounds, initially

produced to substitute previous persistent contaminants, is

also occurring. These emerging contaminants have been

found in all environmental compartments across the

globe [11].

Human exposures and diseases

A hidden aspect that has a fundamental impact on the life

quality of the entire human pop ulation, and possibly its de-

scendants, is exposure to environmental toxicants. Such ex-

posureishiddenbythefactthatmosttimesonecannotbe

* Correspondence: [email protected] Avian Behavioral Genomics and Physiology Group, IFM Biology, LinköpingUniversity, Linköping 58 183, Sweden

© 2015 Guerrero-Bosagna and Jensen; licensee Biomed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use,distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons PublicDomain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in thisarticle, unless otherwise stated.

Guerrero-Bosagna and Jensen Clinical Epigenetics (2015) 7:8 DOI 10.1186/s13148-014-0043-3 aware of our contact with these compounds, which are

numerous and of increasing production and availability.

Worldwide trends show association between environmental

exposures and the incidence of non-infectious diseases [12].

Some of these diseases include the ones observed to be en-

vironmentally induced and transgenerationally transmitted

in rodents, such as obesity, PCOS, or male fertility impair-

ments [4-6,13,14]. For instance, in humans, obesity and

overweight have experienced large increases from 1980

worldwide [15]. Such increase is proposed to be induced by

changes in the environment [16]. PCOS is one of the main

endocrine abnormalities in women, affecting around 7% of

them and associating with reduced pregnancy, diabetes,

obesity, and metabolic and cardiovascular diseases [17].

Although PCOS has been historically regarded as a genetic

disease, recent evidence suggests that it would be mainly

related to early developmental exposures [4], affecting a

shared developmental pathway with metabolic diseases

[17]. Another example is mal e reproductive function.

Trends in human populations consistently show decreasing

male reproductive parameters in the last decades [13,18].

Interestingly, many male reproductive disorders share a

common developmental origin and patho-physiological eti-

ology. These are grouped into the concept of ‘Testicular

Dysgenesis Syndrome ’, which would emerge due to environ-

mental disruption during early testicular development

[13,18]. Therefore, the common factor among these dis-

eases is that they are environmentally induced during early

development. Based on results in rodents, the current high

incidences of these diseases in humans could be correlated

to ancestral exposures to environmental contaminants such

as DDT, BPA, phthalates, or hydrocarbon fumes [5,19].

Food consumption is an important route to environmen-

tal exposures. Recent practices in the food industry derived

from globalization and industrialization have also been

correlated with negative consequences for human health.

Vastly used agro-compounds in clude fungicides or pesti-

cides known to produce transgene rational epigenetic effects

that include developmental, rep roductive, and metabolic ab-

normalities [5,6,20]. Natural estrogenic compounds present

in grains, i.e., phytoestrogens , also gain relevance nowadays,

due to the widespread emergence of soy-based food for both

human and farm animal consumption. Consumption of

phytoestrogens is known to have epigenetic and reproduct-

ive effects [21]. On the side of animal-based food, the in-

tensification of meat product ioninresponsetoagrowing

world population, together with an increased demand for

cheap food in large parts of the world, has caused large pres-

sures on animal welfare on farms [22] and an increased ex-

posure of humans to various pathogens, such as Salmonella

and Campylobacter [23]. In addition, increased exposure to

drug residues from preventive and other treatments of farm

animals is also an issue of concern [23]. Disruption of the

microbiome by inadvertent expo sure to different chemicals

emanating from the animal pr oduction industry may also

affect health and behavior of humans in a range of as yet

poorly investigated ways [24]. Most emphasis on food based

exposures have been on agricu ltural compounds; however,

emphasis should also be placed on animal conditions and

treatments when considering human environmental expo-

sures and the emergence of no n-infectious diseases.

Focus of policies on environmental epigenetics

Today we know that most non-infectious diseases are not

explained by specific genetic va riations but are rather related

to environmental exposures during embryonic development

or infancy [2]. Examples of these diseases include asthma,

allergies, cancers, and obesity. P ossibly, the widespread avail-

ability of environmental contam ination and its future projec-

tions, together with the demonstrated biological possibility

that these exposures can indu ce the onset of transgenera-

tionally transmitted diseases, will have enormous effects in

human health. Therefore, the new knowledge on environ-

mentally induced transgenerat ional epigenetic inheritance

should pose an urgent call for increased regulations on the

production and use of environmental toxicants, as well as

for research evaluating transgenerational effects derived

from these exposures (in both h umans and farm animals). It

is becoming increasingly clear that the quality of life of our

grandchildren depends on our current actions and expo-

sures. In the same way, recent data strongly shows that

many aspects of our health depend on what our grand-

mothers and grandfathers were exposed to in their lives.

Competing interests The authors declare that they have no competing interests.

Authors ’contributions CGB and PJ wrote the manuscript. Both authors read and approved the finalmanuscript.

Acknowledgements The authors greatly appreciate funding support by the European ResearchCouncil Advanced Research Grant Genewell 322206, held by Dr. Per Jensen.

Received: 18 December 2014 Accepted: 26 December 2014

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