Fluctuating Asymmetry As and Indicator of Stress

Emerging Topics in Life Sciences (2022) 6 295–301
https://doi.org/10.1042/ETLS20210274
Review Article
Fluctuating asymmetry as an indicator of stress

Vladimir M. Zakharov and Ilya E. Trofimov
Downloaded from http://portlandpress.com/emergtoplifesci/article-pdf/6/3/295/936963/etls-2021-0274c.pdf by Universidad Nacional Autonoma de Mexico (UNAM) user on 02 October 2022
Koltzov Institute of Developmental Biology of the Russian Academy of Sciences, 26 Vavilov Street, Moscow 119334, Russia
Correspondence: Ilya E. Trofimov (trofimov@ecopolicy.ru)
Fluctuating asymmetry as a special kind of asymmetry can be defined as deviations from

a known predetermined ratio of the parts of morphological structure under study. As a
special type of phenotypic variability fluctuating asymmetry is a manifestation of onto-
genetic noise or developmental variability. This type of variability is ubiquitous and plays
a significant role in the observed phenotypic diversity. The level of fluctuating asymmetry
turns out to be an indicator of optimal developmental conditions and genetic coadapta-
tion. It is also considered as a parameter of fitness. Thus, fluctuating asymmetry acts as
a measure of developmental stability in developmental biology and as a measure of
population condition in population biology.
Introduction
Fluctuating asymmetry study in the laboratory experiments and in natural populations commonly
leads to the conclusion on its dependence on uncommon environmental conditions and genetic coa-
daptation disruption (see [10,17,19,28,43,47] for a review). The aim of this study is to highlight the
main reasons for justification of the statement on fluctuating asymmetry as an indicator of stress in a
broader sense. The justification is based on the characteristic of the phenomenon as a kind of asym-
metry (that is an evidence of imperfection of the realization of genetically determined symmetry), as a
type of phenotypic variability (as a result of developmental instability) and as an indicator of bio-
logical system condition (that is morphogenetic measure of health).
Fluctuating asymmetry as a kind of asymmetry

Three main kinds of asymmetry are usually distinguished, including directional asymmetry, antisym-
metry, and fluctuating asymmetry (Figure 1). Directional asymmetry means larger development of the
structure (or higher trait value) on the same side of the body. With antisymmetry, a greater develop-
ment of the structure is observed either on the left or on the right side of the body. Fluctuating asym-
metry is assumed as minor non-directional deviations from perfect symmetry (see [16,20–23,39,47]
for the review of definitions and methodical issues how to distinguish different kinds of asymmetry).
If the first two kinds of asymmetry are associated with significant and genetically determined devia-
tions from symmetry, then fluctuating asymmetry is a consequence of imperfection in the realization
of a determined plan for the morphological structure. Evaluation of the level of fluctuating asymmetry
assumes an assessment of the magnitude of the average difference in the phenotypic expression of a
morphological trait on different sides of the body. Although this phenomenon seems to be insignifi-
cant, it is wide spread and at the certain degree is manifested in all bilateral structures in various
species of living beings [17,19,28,43,47]. The universality of fluctuating asymmetry consists in the fact
that it also takes place even if other forms of asymmetry occur, in this case it is an evidence of the
Received: 4 March 2022 imperfection of the realization of genetically determined asymmetry. As fluctuating asymmetry is
Revised: 11 May 2022 most often assessed in relation to bilateral symmetry, in this study we consider it in these terms as
Accepted: 17 May 2022
well (as it is presented in Figure 1), but it also occurs in relation to other types of symmetry and frac-
Version of Record published: tality [9,10,32]. In a broader sense, this phenomenon can be defined as deviations from a known pre-
5 July 2022 determined ratio of the parts of morphological structure under study.
© 2022 The Author(s). Published by Portland Press Limited on behalf of the Biochemical Society and the Royal Society of Biology 295
Figure 1. Fluctuating asymmetry as a kind of asymmetry.
Fluctuating asymmetry as a type of variability

The phenomenon of fluctuating asymmetry turns out to be even more significant for the concept of phenotypic
variability (Figure 2). These phenotypic differences cannot be attributed to any of the usually considered two
main sources of phenotypic diversity — genetic and environmental ones. Genetic variability refers to pheno-
typic differences associated with differences in the genotype. Environmental variability refers to phenotypic dif-
ferences associated with differences in developmental conditions. Phenotypic differences between the sides of
the body in the case of fluctuating asymmetry appear on the basis of the same genotype under the same envir-
onmental conditions. They are often defined as disturbances in the course of individual development. However,
they actually cannot be considered as disturbances per se. Such differences are rather evidence of some imper-
fection in the realization of genetic information in the course of individual development. Therefore, fluctuating
asymmetry can be considered as developmental noise that reflects the certain level of developmental stability
[18,36,40]. When characterizing the types of variability in terms of their causation, fluctuating asymmetry can
be defined as manifestation of developmental variability, in addition to the usually considered genetic and
environmental variability [2,13,34,47]. This type of variability is expressed in the appearance of phenotypic dif-
ferences in ontogenesis, which cannot be directly referred to genetic or environmental differences. Here again,
as in the characterization of fluctuating asymmetries in the study of kinds of asymmetries, one may get the
impression that this phenomenon is insignificant. And in fact, in many studies it is not specifically considered
and usually refers to something that can be neglected. However, it is not. This phenomenon provides a unique
opportunity to characterize the significance of developmental noise, in relation to different structures under
different conditions.
It turned out that this type of variability is ubiquitous and plays a significant and, in some cases, crucial role
in the observed phenotypic diversity both under experimental conditions and in natural populations of various
species [10,45]. Moreover, given the usual uncertainty about the nature of observed phenotypic diversity, its
elucidation assumes the conduction of special genetic analysis, this type of variability is the only kind of vari-
ability of a known nature, representing developmental noise or developmental variability. This is the signifi-
cance of the study of fluctuating asymmetry, which provides an opportunity for an unambiguous assessment of
this type of variability. As a result, the study of this variability is important for assessing the role of other types
of variability associated with genetic or environmental diversity. The correlation coefficient of trait values on
the left and on the right sides of the body acts as a measure of the ratio of different forms of variability,
increasing from zero, when all observed variability is the result of ontogenetic noise, to 1, as the significance of
other forms of variability, including genetic and environmental ones, increases [27,43]. Such an assessment of
Figure 2. Fluctuating asymmetry as a type of variability.
296 © 2022 The Author(s). Published by Portland Press Limited on behalf of the Biochemical Society and the Royal Society of Biology
the nature of phenotypic diversity is also crucial for the study of the mechanisms of evolutionary transforma-
tions. If under normal conditions in the central part of the species range there is commonly a decrease in the
level of developmental noise and its role in the total phenotypic diversity, then its increase is observed under
unusual conditions in the ecological periphery of the range. A change in the situation associated with a
decrease in the role of ontogenetic noise under unusual conditions can be observed in the course of evolution-
ary transformations, when, due to adaptation, initially non-optimal conditions may become optimal ones. The
result of the transformation can be seen through the comparison of sympatric populations of closely related
species that provides an opportunity to assess the difference in their reaction to the same environmental condi-
tions [45].
Special studies showed that the minimal level of fluctuating asymmetry occurs under the certain conditions,
which can be defined as the optimum. When deviating from these conditions, an increase in developmental
variability is observed. Just like a low noise level is observed only on the basis of genetic co-adaptation, increas-
ing when it is disrupted [5,13,24,30,47]. This indicates the possibility of characterizing this type of variability as
an indicator of optimal developmental conditions and genetic coadaptation. It was also established the relation-
ship between the fluctuating asymmetry level and fitness [6,25,35]. The level of this type of variability turns out
to be reciprocal to the population index of breeding success [44]. From the point of view of developmental
biology, ontogenetic noise acts as a measure of developmental stability. This ontogenetic indicator also acts as a
significant population parameter and opens up an opportunity for the development of population phenoge-
netics or, in a broader sense, population developmental biology associated with the study of developmental
stability in natural populations [12,33,45,47].
Fluctuating asymmetry as an indicator of the biological

system condition
The level of this form of variability allows one to approach the characterization of the condition or health of a
biological system. The condition of a developing organism is characterized by the level of developmental noise,
the condition of biological systems of a higher hierarchical level, from a population to an ecosystem, can be
characterized by the level of developmental noise of its constituent elements, including individuals and popula-
tions of different species (Figure 3). In the case when the assessed impact affects one species, changes in the
studied indicator can be detected only for this species. If the estimated impact, as in the case of anthropogenic
environmental pollution, covers the entire habitat, correlated estimates indicating an increase in the level of
developmental noise are observed for different species of the community, which allows us to approach the char-
acterization of the condition of the biota and the habitat quality. The advantages of this approach to assessing
the condition of the biological system is that it is possible to characterize the degree of deviation of the system
from the optimal condition based on a known norm, as well as the availability of evaluation criteria, which is
often difficult with other approaches. With the accumulation of a sufficiently large amount of data in relation
to the objects under study, it is possible to present an assessment of the situation on a five-point scale of pos-
sible changes in the studied indicator from a normal condition to a critical one. Such a scale was proposed for
the fluctuating asymmetry level of the morphological structures of a number of species from plants to
mammals [41]. It is important that the characteristics of the quality of a biological system and the favorable
environment are carried out in relation to the condition of living beings, including humans. This approach
forms the basis of the methodology for assessing the health of the environment or the health of ecosystem
[11,15,42,45]. The direction seems to be promising within the framework of the concept of one health, which is
Figure 3. Fluctuating asymmetry as an indicator of the biological system condition.
being actively developed today, including the health of humans and other species of living beings, and the
health of the environment [1,3,4].
Assessment of the condition of biological systems based on the study of fluctuating asymmetry seems to be
as rather sensitive and can be applied as an early warning system [14,25,42,45]. This is determined by the
special nature of the phenomenon being evaluated, the phenotypic differences observed in this case are usually
within a certain backlash allowed by natural selection, and their level is a reflection of the condition of the
developing system. At the same time, estimates obtained prove to be essential for characterizing the condition
of the biological system. With an increase in the impact and the degree of deviation from the norm, there is a
connection between the studied indicators of fluctuating asymmetry with other measures of developmental
homeostasis and commonly used indicators of fitness. Such correlated deviations were obtained for genetic,
physiological, biochemical and immunological parameters [45,48]. The significance of the approach associated
with the assessment of fluctuating asymmetry consists in the fact that information on deterioration of develop-
mental stability cannot be obtained using other approaches. Obtaining the necessary information in this case
involves the assessment of structural deviations from the known norm, or developmental noise, in this field the
study of fluctuating asymmetry still is a common measure.
Fluctuating asymmetry as an indicator of stress

As a measure of the condition or health of a biological system, the level of fluctuating asymmetry proves to be
an indicator of stress (Figure 4). Moreover, it turns out to be a non-specific indicator of stress, caused by either
genetic or environmental factors, associated with a change in the condition of the system. First of all, change in
the level of fluctuating asymmetry is observed when deviating from the optimal developmental conditions. As a
result, it becomes possible to characterize stress in the conditions of the ecological periphery of the species
range, at the limit of the distribution of the species, both under natural conditions and under anthropogenic
impact associated with various types of pollution, including climate change [7,8,14,29,38,50]. This opens up the
possibility of monitoring changes in the population condition in the course of population dynamics under
changing environmental conditions and overpopulation impact [44,46]. In addition, the fluctuating asymmetry
acts as an indicator of a change in the population condition in case of deterioration of genetic co-adaptation,
which can occur when the level of homozygosity changes, in the case of hybridization and in the course of evo-
lutionary transformations. This opens up an opportunity to use an approach based on the assessment of fluctu-
ating asymmetry for the characterization of genetic coadaptation by phenotypic variability [5,10,24,45].
Conclusions: significance of fluctuating asymmetry

Fluctuating asymmetry acts as a characteristic of developmental noise, which opens up the possibility of asses-
sing developmental variability, in addition to the commonly considered genetic and environmental variability.
This phenomenon turns out to be as a measure of developmental stability. The phenotypic differences observed
in this case make it possible to approach the characterization of the backlash allowed by natural selection,
which seems important both for the development of the conception of determination of biological processes
and for the practical assessment of the condition of a developing organism in developmental biology. This
ontogenetic indicator also acts as an important parameter in population biology, being of interest here for
assessing the nature of the observed phenotypic diversity, characterizing the condition of the population, and
identifying the mechanisms of evolutionary transformations. The approach is also promising for the population
developmental biology based on the developmental stability study in natural populations. Developmental noise
Figure 4. Fluctuating asymmetry as an indicator of stress.
assessment acts as an indicator of the condition of biological systems, from organism to community, and
characteristics of habitats. This approach can be used as the basis to develop the concept and methodology for
assessing the health of the environment. There is also a potential to conduct special studies of noise, fluctuating
and homeostasis at different levels, from the gene network to the organism, population and community
[26,31,37]. Against the background of the development of modern molecular genetic areas, including the field
of epigenetics, the assessment of fluctuating asymmetry provides an opportunity to characterize ontogenetic
noise, which seems difficult for other approaches. This unique phenomenon is still waiting for its detailed
study; its evaluation seems promising for solving a wide range of different problems both in theory and in
practice.
Summary
• Fluctuating asymmetry is a tool to study the role of developmental variation in the total pheno-
typic diversity.
• Fluctuating asymmetry is a developmental noise within the limits of the certain backlash in
realization of genetic information in ontogeny allowed by natural selection.
• Fluctuating asymmetry is also a population parameter to characterize possible spatial and

temporal dynamics of phenotypic diversity and population condition.
• An increase in fluctuating asymmetry level proves to be an early warning system to monitor

the biological system and habitat quality.
Competing Interests
The authors declare that there are no competing interests associated with the manuscript.
Funding
This work has been funded by Government program of basic research in Koltzov Institute of Developmental
Biology of the Russian Academy of Sciences in 2022 № 0088-2021-0019.
Author Contributions
The article was prepared at all stages, from the beginning to the end, including the reaction to the reviewers’
comments and suggestions, in collaboration of all authors V.M.Z. and I.E.T. All authors have read and agreed to
the published version of the manuscript.
Acknowledgements
We thank the members of the laboratory of postnatal ontogenesis of the Koltzov Institute of Developmental
Biology of the Russian Academy of Sciences for a fruitful cooperation.
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Emerging Topics in Life Sciences (2022) 6 295–301

Fluctuating asymmetry as an indicator of stress

Fluctuating asymmetry as a special kind of asymmetry can be deﬁned as deviations from

Fluctuating asymmetry as a kind of asymmetry

Fluctuating asymmetry as a type of variability

Figure 2. Fluctuating asymmetry as a type of variability.

Fluctuating asymmetry as an indicator of the biological

Figure 3. Fluctuating asymmetry as an indicator of the biological system condition.

Fluctuating asymmetry as an indicator of stress

Conclusions: signiﬁcance of ﬂuctuating asymmetry

Figure 4. Fluctuating asymmetry as an indicator of stress.

• Fluctuating asymmetry is also a population parameter to characterize possible spatial and

• An increase in ﬂuctuating asymmetry level proves to be an early warning system to monitor

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