Biol. Rev. (2013), 88, pp. 476–489.

476
doi: 10.1111/brv.12006

Temperature-size relations from the

cellular-genomic perspective
Dag O. Hessen1,∗ , Martin Daufresne2 and Hans P. Leinaas3
1
Department of Biology, University of Oslo, CEES, PO Box 1066 Blindern, 0316, Oslo, Norway
2 HYAX-EL, Irstea, 3275 Route de Cézanne, 13182, Aix-en-Provence, France
3
Department of Biology, University of Oslo, Integrative Biology, PO Box 1066 Blindern, 0316, Oslo, Norway

ABSTRACT

A family of empirically based ecological ‘rules’, collectively known as temperature-size rules, predicts larger body size in
colder environments. This prediction is based on studies demonstrating that a wide range of ectotherms show increased
body size, cell size or genome size in low-temperature habitats, or that individuals raised at low temperature become
larger than conspecifics raised at higher temperature. There is thus a potential for reduction in size with global warming,
affecting all levels from cell volume to body size, community composition and food webs. Increased body size may be
obtained either by increasing the size or number of cells. Processes leading to changed cell size are of great interest from
an ecological, physiological and evolutionary perspective. Cell size scales with fundamental properties such as genome
size, growth rate, protein synthesis rates and metabolic activity, although the causal directions of these correlations are
not clear. Changes in genome size will thus, in many cases, not only affect cell or body size, but also life-cycle strategies.
Symmetrically, evolutionary drivers of life-history strategies may impact growth rate and thus cell size, genome size
and metabolic rates. Although this goes to the core of many ecological processes, it is hard to move from correlations
to causations. To the extent that temperature-driven changes in genome size result in significant differences among
populations in body size, allometry or life-cycle events such as mating season, it could serve as a fast route to speciation.
We offer here a novel perspective on the temperature-size rules from a ‘bottom-up’ perspective: how temperature
may induce changes in genome size, and thus implicitly in cell size and body size of metazoans. Alternatively: how
temperature-driven enlargement of cells also dictates genome-size expansion to maintain the genome-size to cell-volume
ratio. We then discuss the different evolutionary drivers in aquatic versus terrestrial systems, and whether it is possible
to arrive at a unifying theory that also may serve as a predictive tool related to temperature changes. This, we believe,
will offer an updated review of a basic concept in ecology, and novel perspectives on the basic biological responses to
temperature changes from a genomic perspective.

Key words: temperature-size rules, genome size, body size, gigantism, polyploidy, global warming.

CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 477
II. Determinants of size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 478
(1) Cell size versus cell number . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 478
(2) Cell size and genome size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 479
(3) Unifying patterns across taxa? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 480
III. Genome Expansion by polyploidy or by accumulation of noncoding Dna . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 481
(1) Polyploidization and endopolyploidy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 481
(2) Diploid genome size variation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 481
IV. Cell size, genome size, growth and metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 483
V. Alternative evolutionary drivers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 484
(1) Life-cycle effects and inversed TSR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 484
(2) Nutrition and diffusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 484

* Address for correspondence (Tel: +47 22854553; Fax: +47 22854001; E-mail: dag.hessen@bio.uio.no.)

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Genome size and temperature in ectotherms 477

(3) Predation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 485

(4) Effect of population size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 485
VI. Global-change implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 485
VII. Future directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 486
VIII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 487
IX. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 487
X. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 487

I. INTRODUCTION 2008; Yom-Tov & Geffen, 2011; Yvon-Durocher et al.,

2011). Thus, it is generally important to distinguish between
All phenomena in nature and traits in organisms obviously geographical patterns related to climate clines and direct
have their specific causes, however in many cases the various responses to temperature, and although we will focus
drivers of a given phenomenon are so complex that it is hard our review of thermal responses in this context, we will
to arrive at universal and deterministic predictions, not to also discuss possible roles of such potentially confounding
say laws (see e.g. Peters, 1983; Lawton, 1999, for discussion). factors.
Nevertheless, the search for universal patterns and It is also important to realize that different habitats and
explanations has a strong appeal, and there is a long tradition different life-cycle properties may yield different responses
in ecology of establishing various ‘laws’, often based on along temperature or geographical clines, and that conflicting
correlative observations. When put under scrutiny, such laws opinions on the generality and causality behind Bergmann’s
often turn out to be different phenomena that are lumped into rule and other climate-body size relations may partly reflect
specific categories due to their superficial resemblance. They such differences (e.g. Watt et al., 2010). In particular,
can only rarely be nailed to basic physical or first principles. among terrestrial invertebrates an opposite trend appears
While the pitfalls are obvious, the fruitfulness of this tradition to be common; i.e. the converse Bergmann cline with
is in the underlying synthesis: revealing patterns that call for reduced body size in colder areas. Many of these apparently
analyses of causation. The tendency of overselling observed contradictory findings should be seen in the light of life-
patterns into ecological rules may result in discussions about history traits and adaptations (Chown & Gaston, 2010), and
the rule itself, e.g. criticism versus defence, rather than the we will explore these issues towards the end of this review.
causations underlying the patterns. In addition to the observed pattern of body size along
The Bergmann rule served as a point of departure for climate gradients, experimental studies have shown that
most later work on temperature-size relationships. This rule developmental temperature may affect adult size across a
linked body size of endothermic species to the thermal wide range of ectotherms from protists to fish, i.e. that indi-
environment in which they lived (Bergmann, 1847). The viduals raised at low temperatures generally grow slower but
argument was based upon the mass-specific heat loss being finally become larger than their conspecifics raised at higher
dependent on body volume to surface area ratios, and thereby temperature. As a consequence the growth trajectories under
favouring larger body size in cold environments. The original cold versus warm conditions should cross somewhere during
Bergmann’s rule dealt specifically with endotherms at the ontogeny (Arendt, 2007). This phenomenon, which thus
interspecific level (Watt, Mitchell & Salewski, 2010). The differs principally from temperature-cline rules, has been
first digression from the Bergmann rule was to consider labeled the temperature-size rule (TSR) (Atkinson, 1994;
its relevance at the intra-specific scale; a pattern generally Angilletta et al., 2004; Atkinson, Morley & Hughes, 2006;
referred to as James’ rule (James, 1970). Since then, enlarged Karl & Fisher, 2008; Daufresne, Lengfellner & Sommer,
body size in colder areas has also been documented by 2009). Even though the underlying mechanisms are still
several studies on ectotherm metazoans (Atkinson, 1994; debated, the TSR suggests that, with regard to ectotherms,
Timoteev, 2001; Angilletta, Steury & Sears, 2004). While the observed geographical clines in body size are, at least
somewhat imprecise, these patterns have also been included partially, due to temperature per se and not simply to thermal
in the concept of Bergmann’s rule or Bergmann clines. covariates like duration of the growth season or nutrient
The causation of such clines in ectotherms obviously differs abundance.
fundamentally from those originally explaining the rule in The great variations among species and populations in
endotherms, and in addition there has been an increasing how climate-related body-size differences are expressed
focus on intraspecific patterns (Chown & Gaston, 2010). emphasize that several independent triggers and mechanisms
The arguments of the original Bergmann’s rule were may be involved. Thus, despite their apparent familiarity,
directly linked to ambient temperature. However, many case these empirically obtained patterns of claimed rules
studies following the Bergmann tradition address patterns should rather be seen as a concept cluster (Watt et al.,
along eco-geographical clines where temperature per se is only 2010). Accordingly, Angilletta et al. (2004) argued for the
one of several potential triggers of body size variability. Such development of a unifying multivariate theory, focusing
confounding factors may include size-selective predation, on adaptive coevolution of thermal reaction norms for
nutrient regimes and gas diffusion (Clarke, 2003; Kaartvedt, growth rate and size at maturity. However, such a unifying

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478 D. O. Hessen and others

model may become too general for analyzing the underlying Community size changes
mechanisms of very different phenomena. Moreover, from
a thermal point of view it is still unclear to what extent
phenotypic responses to developmental temperature may
represent non-adaptive effects at cellular or molecular levels

Predation Nutrients
(e.g. Von Bertalanffy, 1957; Van der Have & de Jong, 1996), Body size changes Food web/
and if non-adaptive effects of temperature may secondarily productivity
have selective consequences.
In this review we select another approach to the problem Cell numbers
of disentangling phenotypic plasticity from evolutionary
changes, and of thermal triggers from non-thermal, by
focusing on the cellular and genomic perspective. We also Cell size

Temperature
apply this ‘bottom-up’ approach primarily to unicellular
eukaryotes and ectotherms as the vast majority of organisms
are either unicellular or invertebrates, and also because Polyploidy
ultimately body size is determined either by the number of
cells, their size, or both. Genome size is important in this Genome size
context as a covariate and potential determinant of cell size
– and thus potentially body size. This perspective differs
from adaptive explanations where body size in itself acts Life history
as the selective trait (Angilletta et al., 2004). These views Cell division/
growth rate/ Speciation Food web/
are not mutually exclusive since changes in body size may metabolic rate productivity
secondarily have consequences for cell and genome size.
It should also be equally relevant both in the context of Fig. 1. Conceptual flow-chart for drivers and effects related to
adaptive responses along temperature clines and the more temperature–size responses, which also describes the structure
immediate TSR. Moreover, it is relevant both at the intra- of this review. Core drivers and responses focused in this
context are given as bold lines. Temperature and potentially
and interspecific level. confounding factors such as predation and nutrients may directly
The following review is structured along the lines depicted and indirectly affect community-size structure, body size, cell
in Fig. 1, where the main drivers and responses are given size and genome size. These hierarchical levels may also be
in bold. Our point of departure is the direct effects of causally linked both by ‘top-down’ and ‘bottom-up’ processes.
temperature at the genomic and cellular level. From here we
continue by discussing the relationship between cell size and
body size in multicellular ectotherms, e.g. to what extent do 2012). It should be noted, however, that these (and other)
metazoans grow by increase in cell number or cell size? We recent papers addressing temperature responses partly deal
will here primarily pursue growth by increasing cell size since with responses at the community level (shifts in species or
this represents the ultimate link between genome size and stages), partly with long-term evolutionary adaptations along
body size. We will also focus on ectotherms since they, by temperature clines, and partly with species-specific body-size
contrast with endotherms, display a remarkable variability responses to temperature within their life cycle.
in genome size (Gregory, 2005). We then evaluate external A better understanding of temperature-size relations at
versus internal drivers of changes in cell size. In particular, the various levels and in various ecosystems is therefore a
apparent coupling between genome size and cell size, and the prerequisite for predictions of ecosystem responses to climate-
potential causal links between these relationships. We further change effects, and clearly understanding basic responses at
discuss the different evolutionary drivers, e.g. physiological the genome and cellular level may provide insights into
temperature adaptations versus life-history traits, which may processes at higher hierarchical levels.
explain differences between aquatic and terrestrial systems.
Lastly, we address some potential large-scale ecosystem
consequences of thermal responses of body size. II. DETERMINANTS OF SIZE
Since so many ecological and biological properties scale
with body size, the current and predicted rise in global
(1) Cell size versus cell number
temperature will likely have far-reaching consequences to
the extent that it affects size at all levels from the genome to Individual body growth may occur either by increasing cell
the community level. If there are fundamental physiological size or cell number (Timoteev, 2001; Arendt, 2007), or
principles linking temperature and size, then one would through ‘mixed strategies’ (Fig. 2). Few taxa have fixed cell
expect reduced size with elevated temperatures, as indeed numbers throughout their life, and increased cell number is
has been suggested by recent studies (Atkinson, Ciotti & likely to be an important component of growth (Peters, 1983;
Montagnes, 2003; Daufresne et al., 2009; Gardner et al., Stevenson, Hill & Bryant, 1995; Arendt, 2007). However
2011; Sheridan & Bickford, 2011; Forster, Hirst & Esteban, for both organisms with variable and fixed cell numbers,

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Genome size and temperature in ectotherms 479

(A) (B) has been explicitly linked to increased cell size, while
conspecific populations sampled across climatic gradients,

Cell or genome size

Higher and lower levels
c
show increased body size in cooler environments mainly
b attributed to increased cell numbers (Partridge et al., 1994;
a French, Feast & Partridge, 1998). We still have limited
Inter or intraspecific 3 knowledge on how cell size versus cell numbers varies within
species, between species or between taxa. This is an important
Cell or genome size

Body size
issue, because if this varies between related species or between
2 (C) conspecific populations that show similar overall increase in
body size at lower temperature, body size is most likely the

Cell or genome size

Within-species level target of selection since it apparently is obtained by different
1
mechanisms. If, on the other hand, cell size co-varies with
body size within taxa, then selection might also work on cell
size or some sub-cellular structures, such as genome size.
Body size

Body size (2) Cell size and genome size

Fig. 2. Potential relationships between cell or genome size So far, partly due to methodological challenges and laborious
and body size. (A) Body size increase is simply by increase in procedures, there are few studies describing variations in cell
cell number (1); by a combination of increased cell numbers size within and among species. However, in most cases,
and cell size by genome size expansion or endopolyploidy (2); analysis of genome size (or eventually nucleus size) may serve
or by increase in cell size (3). Modified from Kozlowski et al. as a good proxy of cell size – and in itself serve as the
(2003). (B) Potentially different slopes for cell or genome size main driver of cell size. A strong positive correlation between
versus body size at different taxonomic levels (e.g. classes a, b genome size and cell size appears to be rather universal
and c within a given phylum or order). a, b and c within a in both plants and animals (Cavalier-Smith, 1978; Bennett,
given class may yield different slopes compared with the higher 1987; Gregory, Hebert & Kolasa, 2000; Gregory, 2005),
level, reflecting different evolutionary strategies and drivers. (C)
particularly at higher taxonomic levels (Starostova et al.,
Allometric effects in cell or genome size versus body size may
occur during ontogeny, e.g. by somatic endopolyploidy. 2009). The causality is not clear, however, and may work
in both directions (Hessen et al., 2010). The relationship is
less settled for vertebrates, although in vertebrate ectotherms
variation in body size may partly be attributed to changes in such as fish there is a close coupling between genome size
cell size. Similarly, differences in adult body size among and erythrocyte size, and erythrocyte size represents a good
individuals and populations, or between closely related proxy for general somatic cell size (Gregory, 2005). The
species are caused either by differences in cell number or mechanistic coupling between these metrics is also supported
cell size. In principle, growth during certain life stages, e.g. by the observation that experimental expansion of genome
until maturity, may be determined primarily by cell number. size causes increased cell size (Gregory, 2001). However,
For organisms with indeterminate size, final adult body size increased cell size favouring enlargement of the genome is
could rely more on cell volume. also a likely, but not yet tested, scenario.
For a wide range of ectothermic metazoans it has Genome size may increase by two principally different
been demonstrated that individuals reared under reduced routes: either an increase in number of base pairs (normally
temperatures reach larger cell sizes than conspecifics reared in the intron regions), causing larger diploid (and haploid)
at higher temperatures (Robertson, 1959; van Voorhies, genomes, or by partial or whole-genome duplication events,
1996; Arendt, 2007; Kammenga et al., 2007; Daufresne the latter being known as polyploidization. However,
et al., 2009). This fits the argument from van der Have & genome structure that affects nuclear volume, e.g. chromatin
De Jong (1996), that cell growth is more sensitive to thermal packaging, mitotic processes or aneuploidy (chromosome
constraints than is cell division, meaning that organisms number anomalies) may also affect cell volume. Both on
with a rather constant cell number would be smaller due to the intra- and interspecific levels it is well documented that
reduced cell size at elevated temperatures. A fundamental increases in genome size through polyploidization generally
question is whether such differences in thermal sensitivity result in increased cell size (Gregory, 2005). While both
reflect ultimate or proximate causations; i.e. is it an innate increased diploid genome size and polyploidization are
property of the processes, or a mechanism reflecting a potential means of increasing cell size, and both seem
favoured thermal response of cell size? somehow related to low temperatures, the evolutionary
For organisms with fixed cell number (e.g. nematodes drivers may be widely different and occur at different time
and rotifers), body growth obviously can only occur through scales. We will thus address both of these mechanisms, but
changes in cell size, while the situation is more complex first and foremost consider changes at the chromosome level,
in organisms with variable cell numbers. In Drosophila i.e. in diploid or haploid genome size.
melanogaster, the observed phenotypic response of increased Genome size may, for the reasons given above, serve
adult body size at lower developmental temperatures as a proxy of cell size, and far more estimates of genome

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480 D. O. Hessen and others

size than cell size are available. The positive correlation

between genome size and body size among invertebrate taxa Calanus hyperboreus (12)
(McLaren, Sevigny & Corkett, 1988; Ferrari & Rai, 1989;
Finston, Hebert & Footit, 1995; Gregory, 2005; Rasch &
Wyngaard, 2006) indicates that the contribution from cell
size to the difference in body size between related species may
be more significant, at least in invertebrates, than hitherto
recognized.
The explicit coupling between low temperature and large
genome and body size typically found in many marine
invertebrates is of note in this context (Atkinson, 1994; Calanusglacialis (10)

Timoteev, 2001; Rees et al., 2007, 2008; Hessen & Persson,

2009). This may be seen even between closely related species
such as the three dominant species of calanoid copepods Calanus finmarchicus (6)

in northern, marine waters, Calanus finmarchicus, C. glacialis

and C. hyberboreus (see appendix in Hessen & Persson, 2009).
Fig. 3. Example of three closely related marine copepod
These species have body-size differences that correlate with
species that show both a body-size and genome-size variability
genome size, and the latitudinal temperature cline (Fig. 3). along a temperature gradient, with the larger species living
Populations of C. glacialis, living under different temperature in the coldest waters and also having the lowest growth
regimes, have also been found to differ both in genome and rate and most prolonged life cycle. Average genome size
body size, with the largest genome and body size at the in pg DNA cell−1 (in parentheses) is from the Animal Size
lowest ambient temperatures (H.P. Leinaas, D.O. Hessen & Database: http://www.genomesize.com/. Photo courtesy of
M. Jalal, unpublished data). Since interspecific differences Janne Søreide.
in genome size versus body size yield a positive slope in
copepods as for other major groups of crustaceans, except
(A) (B)
decapods (Hessen & Persson, 2009; Fig. 4), this suggests 2 50
that cell size indeed plays a major role in these body size
differences at the interspecific level for major groups of 1 10
crustaceans. This is supported by the fact that copepods,
at least for part of their life cycle, seem to have fixed cell
numbers (McLaren & Marcogliese, 1983), meaning that
Haploid DNA (pg cell–1)

1
at the intraspecific level they can also only increase their
volume by means of increased cell size. The lack of positive 0.2 0.2
correlation in decapods (Fig. 4D) may reflect that the body 0.5 1 10 0.5 1 10

plan in this group is too diverse to reveal positive slopes at (C) (D)
100 50
this aggregated level, or that interspecific differences in body
size primarily reflect differences in cell numbers.
10 10
(3) Unifying patterns across taxa?
To maintain a realistic scope for our review, we will focus on
metazoan ectotherms, and for reasons given in Section I, do 1

not include endotherms (or prokaryotes) in this context. It 0.5 1

10 50 10 100 1000
is worth considering, however, whether or not similar TSRs Body size (mm)
occur across taxa or ecosystems, and, if so, whether this
reflects unifying drivers. The basic question is thus whether Fig. 4. Genome size versus body size for major groups of
autotrophs and heterotrophs, protists and metazoans follow crustaceans. (A) cladocerans; (B) cyclopoid copepods (open
the same patterns and adhere to the same ‘laws’. circles) and calanoid copepods (filled circles); (C) amphipods;
(D) decapods (crabs = open circles, lobsters = open triangles,
TSRs in protists are interesting because they represent crayfish = filled circles, shrimps = open squares, prawns = filled
a strictly cellular response, unlike metazoans, where size triangles). Adapted from Hessen & Persson (2009).
responses also may involve changed cell numbers. In a
comprehensive study, Atkinson et al. (2003) compared a
range of protists and found a linear decrease in size with with increasing temperatures (Section VI), although the jury
temperature (2.5% ◦ C−1 ), irrespective of habitat (marine, is still out as to whether this reflects intraspecific changes
brackish or fresh water) or nutrition (heterotrophs or in size, species replacement or both, but the trend seems
autotrophs). The same phenomenon was reported by Forster to be consistent for both autotrophs and heterotrophs. The
et al. (2012). There are also several studies suggesting fact that the TSR holds for single cells suggests that the
decreased cell size at the community level among protists causal direction may not necessarily be from body to cells.

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Genome size and temperature in ectotherms 481

Rather, we would argue that the causal direction often is low temperatures directly promote polyploidy is not known.
the opposite. Unfortunately, these protist studies are not Interestingly, polyploidy may not only be an inherent trait
accompanied by genome size estimates. For vascular plants, along temperature clines, but also at least for endopolyploidy,
the issue is complicated by many confounding factors, such may be related to ontogeny (Beaton & Hebert 1989; Beaton
as nutrient and water availability, insolation and physical & Hebert, 1994), and perhaps is also inducible, e.g. by
stress. There is no doubt a general trend towards smaller size temperature or predation risk (Beaton & Hebert, 1997).
with altitude and latitude; while at the same time there is Generally, polyploids have slower growth and delayed
an increasing incidence of polyploidy along the same clines, developmental rates compared with their diploid conspecifics
indicating larger cells (Section III.1). at standard culturing temperatures (e.g. 15–20◦ C), probably
For marine ectotherm metazoans, notably the inverte- owing to their enlarged cell size and slower cell division
brates, we will argue that the general observation of enlarged (Weider, 1987). They also generally attain larger size as
adult body size at low temperature reflects enlarged cell and adults. The reduced growth rate in polyploids could indicate
genome size, governed by the same processes as for protists. that this trait is not fitness-promoting per se, but rather a
For terrestrial invertebrates that complete their life cycle ‘by-product’ of something else. Under low temperatures,
within a brief season, we may see different responses, includ- however, polyploid members of the Daphnia pulex complex
ing both larger and smaller body size in colder areas (see grow and mature faster than their diploid counterparts
Section V.2). The key point, however, is the general correla- (Dufresne & Hebert, 1998; Van Geest et al., 2010), suggesting
tion between genome size and cell volume, which seems to that selection in favour of gene duplication or polyploidy in
be valid among taxa and habitat. This means that whatever fact could promote fitness at low temperatures by enhancing
the cause might be, changes in cell volume will likely cause enzyme expression or protein synthesis. Increased gene
changes in genome size and vice versa. This will have fun- dosage in certain high-ploidy tissues is typical of cells involved
damental consequences for a range of life-cycle attributes, in secretion or intense protein production (Gregory & Hebert,
especially growth rate and metabolism. For a number of 1999). For example, the highest level of endopolyploidy
invertebrates, we will also argue that these properties are observed to date, exceeding one-million-ploid, occurs in
also determinants of body size. the silk-producing glands of the larval silkworm moth,
Bombyx mori (Perdix-Gillot, 1979), which has undergone
intensive artificial selection over long periods to maximize
silk production. The detailed studies of metabolic pathways
III. GENOME EXPANSION BY POLYPLOIDY OR in Daphnia pulex clearly demonstrate an ‘ecoresponsive
BY ACCUMULATION OF NONCODING DNA genome’ where the maintenance of duplicated genes is not
random, and the analysis of gene expression under different
(1) Polyploidization and endopolyploidy environmental conditions revealed that numerous paralogs
acquire divergent expression patterns soon after duplication
The observed pattern of variation in genome size at the
(Colbourne et al., 2011). Also in functional diploids, gene
haploid or diploid level is primarily related to accumulation
amplification may serve as way of boosting expression of
of various introns; i.e. repetitive noncoding sequences, trans-
key enzymes at low temperatures (Harding, Anderberg &
posons and retrotransposons (e.g. Gregory, 2001; Lynch, Haymet, 2003; Carginale et al., 2004)
2007). However, cell size may also increase by gene dupli- While polyploidy is regarded as an adaptation to low
cations or partial or full chromosome duplication. Actually, temperature and extreme environments, it is also associated
post-duplication downscaling events may lead to genome with increased incidence of asexual reproduction (Otto &
size differences also in functional diploids, but for practical Whitton, 2000; Brochmann et al., 2004) since increased
reasons, these two routes to genome size variations (and thus chromosome number would not conflict with recombi-
cell- and body-size variations) should be treated separately. nation, and more copies may also form a kind of allelic
For organisms growing by fixed cell number, such as backup to buffer against lethal mutations in the absence of
probably most nematodes and rotifers, enlargement of the recombination. Hence, in the case of polyploidy, climate
cells seems to happen primarily via increased levels of cline patterns might, at least partially, represent an indirect
endopolyploidy, i.e. an increase in ploidy levels in certain effect of increased incidence of asexual reproduction in cold
tissues (van Voorhies, 1996; Kammenga et al., 2007). Somatic environments. In any case, it is important to differentiate
endopolyploidy, however, seems to occur to some extent between partial or full duplication events and the accumula-
in most organisms that also are functionally diploid (with tion of non-coding DNA as two different routes to increase
haploid gametes). Small invertebrate and facultative asexuals genome size although both may cause enlargement of cell
like Daphnia spp. may have highly tissue-specific ploidy levels size. In the following, we will mainly focus on drivers and
that exceed a 1000-fold increase in chromosome copies mechanisms for genome expansions at the diploid level.
in certain tissues, and somatic ploidy levels that may also
increase with ontogeny (Beaton & Hebert, 1994). Typically,
(2) Diploid genome size variation
the incidence of polyploidy also increases at high latitudes
and lower temperatures (Weider, 1987; Otto & Whitton, While ectotherms possess a striking variability in genome
2000; Brochmann et al., 2004), although the extent to which size even within closely related species, endotherms only

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482 D. O. Hessen and others

2.2
130
response via this mechanism works directly on the cell size,
2.1
Birds Fish
120 a persistent change in temperature may subsequently lead to
2 110 a selective advantage of a corresponding change in genome
1.9 100 size. Similarly, if there are selective drivers for accumulation

............................................
1.8 90
1.7
of introns and thus enlarged diploid genomes, increased cell
80
1.6 70
size (and thus body size in metazoans) would be expected to
1.5 60 result as a secondary consequence.
1.4 50 The fact that intraspecific variability in genome size
1.3 40 may be induced experimentally over a few generations
1.2 30 in copepods (Escribano, McLaren & Klein Breteler, 1992)
Haploid DNA (pgcell-1)

1.1 20
1 10
suggests that evolution of genome size may be rapid. This
0.9 0 is also supported by the fact that in Drosophilida the
genome size appears to have increased successively during
their geographic expansion due to increased prevalence of
20 transposons (Vieira et al., 2002), and in Daphnia pulex recent
8
Mammals Insects
and rapid intron gains have also been reported (Li et al.,
7 2009). In addition, recent experiments have demonstrated
not only increased mature body size in Daphnia species raised
6 at 10◦ C relative to 20◦ C, but also increased nucleus size
5 10 as revealed by flow cytometry. This is likely caused by
..................................

temperature changes in chromatin packing (M. Jalal & D.

4 O. Hessen, in preparation). In principle, changes in gene-
copy number could induce rapid changes in genome size
3
in response to ambient drivers, but whether this can occur
during a single life span is not settled. Independent of whether
.......

2
0 increase in genome size is a secondary response to increase
Frequency distribution in cell size, or vice versa, selection at the genome level must
be part of the overall dynamics. Otherwise, the observed
Fig. 5. Examples of species genome size distribution within relationship between genome size and cell size could not be
two major groups of homeotherms (birds and mammals) established.
and ectotherms (fish and insects). Left panels represents
It is again worth stressing that any genome size increase
frequency distribution, right panel is median (line) 5%
percentiles (diamonds), 25 and 75% percentiles extension at low temperature may not necessarily be an adaptive trait,
of boxes and 95% percentile (extension of dotted line). but could reflect a passive response accumulation by ‘selfish
Values outside 95 percentiles are represented as single dots. DNA’, e.g. by transposon proliferation simply because there
Bracket corresponds to box extension based on means. Note is a low counter-selective pressure at low growth rate. In this
the difference in scales. Source: Animal Genome Database case only intron-level fitness is relevant. In fact the question
http://www.genomesize.com/ (Gregory, 2012). whether TSRs reflect fitness-promoting responses or not is
the fundamental issue, and we will address this issue below
possess small variations (Fig. 5 Gregory, 2005). This from various angles.
difference between endo- and ectotherms could thus be The distinction between genotypic and phenotypic traits
in itself indicative of a temperature effect. Both analyses is fundamental in evolutionary and ecological contexts.
of genome size in relation to environmental temperature, Initially, the distinction is straightforward. However, the
and experimental studies of the effect of developmental long-term phenotypic responses along temperature clines
temperatures, support the view that increased cell size (e.g. Bergmann-type clines) represent evolved, genotypic
is a widespread response to low temperatures (Arendt, traits, while the more immediate responses within a
2007). Given that genome size and cell volume are tightly lifetime are perceived as phenotypic responses. In addition,
and causally related (Cavalier-Smith, 1978, 1985; Bennett, phenotypic plasticity in morphology, physiology and life
1987; Gregory, 2005), this raises the following fundamental cycles represent evolved traits. Flexible traits come at some
questions: how can animals grow by increasing their cell size costs, but for organisms living in variable environments, the
if this implies a corresponding disturbance of the assumed ability to make rapid adjustments is vital.
regulation of cell size versus genome size? What is the causal In the following one should bear in mind that immediate
direction between genome size and cell size? Could there responses represent evolved traits. For the issue of genome
be a reciprocal regulation of cell size and genome size? To size per se, the distinction between genotypic and phenotypic
address these questions it is crucial to assess whether cells can responses is even more subtle. Given that increased genome
increase in size without a corresponding increase in genome size by accumulation of transposons represents a response to
size, e.g. by cytoplasmic expansion, and how fast the genome changes in phenotypic traits such as increased cell volume, it
size may respond to the resulting mismatch. If the phenotypic could be seen as a phenotypic response at the genome level.

Biological Reviews 88 (2013) 476–489 © 2012 The Authors. Biological Reviews © 2012 Cambridge Philosophical Society
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Genome size and temperature in ectotherms 483

IV. CELL SIZE, GENOME SIZE, GROWTH AND (this has been used as an argument for reduced body
METABOLISM size at high latitudes). On the other hand, mass-specific
metabolism decreases with increasing mass, meaning that
If we accept the premise that larger genomes generally large organisms can maintain a higher biomass under
lead to larger cells, the increase in genome size with periods of starvation. Predictable periods of starvation is
decreasing temperature is likely to have consequences for typical for many cold environments, and thus may result
metabolism (Starostova et al., 2009). For a given body in patterns in agreement with TSRs. Examples of this are
temperature, genome size generally correlates negatively systems characterized by ‘feast and famine’ cycles, with
with growth rate across both plants and animals (Bennett, brief periods of high productivity followed by extended
1987; Gregory, 2005), and in animals also with mass-specific post-bloom periods with low productivity (Chapelle, Peck
metabolic rate (Kozlowski, Konarzewski & Gawelczyk, 2003; & Clarke, 1994). Thus, superimposed on general effects of
Gregory, 2005). Developmental rate has also been found temperature on metabolism are drivers that may be directly
to be negatively associated with genome size in several or indirectly linked to the temperature/climate and thus
invertebrates; such as polychaetes (Gambi et al., 1997) obscure causations. One should also bear in mind that
copepods (White & McLaren, 2000; Wyngaard et al., 2005) allometric response in basic resting and active metabolic rate
and Drosophilidae (Gregory & Johnston, 2008). This also may respond differently to temperature, but to reveal these
holds true for some ectothermic vertebrates, for example issues fully is beyond our scope herein.
Maciak et al. (2011) reported an inverse relationship between Independent of temperature, downsizing or streamlining
standard metabolic rate and erythrocyte and genome size in of genomes can be seen as a selection to gear up growth
fish. Additionally, cell division rate is coupled to metabolic rate (Gregory et al., 2000; Gregory, 2001, 2005; Hessen
rate and nutrient availability (Hall, Raff & Thomas, 2004; et al., 2010). In comparison, it is much harder to come up
Savage et al., 2007). Thus small genomes should be correlated with fitness-promoting aspects of larger cells per se since this
with high growth and high metabolic activity, which indeed ultimately would slow down growth. Kozlowski, Czarnoleski
often seems to be the case (Wagner, Durbin & Buckley, & Danko (2004) argued however that production based on
1998). From a growth-rate perspective, it is therefore easy to size-dependence resource acquisition and metabolic rates
come up with evolutionary drivers for reduced genome and may explain optimal allocation to growth versus reproduction
cell size, although it is not straightforward to explain direct consistent with TSRs, and that TSRs thus reflect an adaptive
selection for larger genomes and cells. trait. Most important in this context is their argument that
A crucial part of the current discussion on temperature-size low temperature is not only a proximate, but also an ultimate
relationships is to what extent observed patterns are adaptive, cause of enlarged body size, since it is difficult to imagine that
i.e. may be explained from their fitness consequences mechanisms compensating the increase in body size would
(Angilletta et al., 2004). In this context the effects of body not evolve if larger body size in the cold decreased fitness.
size (Brown et al., 2004; Gillooly et al., 2005), or cell Kozlowski et al. (2004) and Starostova et al. (2009) also argue
and genome size (Xia, 1995; Kozlowski et al., 2003) on that under strong selection for increased body size, increased
metabolism and biosynthesis is highly relevant. Temperature cell size could be favoured as a means of reducing metabolic
and body mass are linked through metabolic activity, but costs of maintenance. Hence larger cells could be a result of
again there are contrasting opinions on the causal relations selection operating at the cellular level, while smaller cells
(Isaac & Carbone, 2010). A three fourth allometric exponent could be a result of selection both at the cellular and body
for metabolic rate versus body size, relating to the fractal level. Such mechanisms could operate both in the long term
branching of supply systems to the body with increased (e.g. creating size patterns along temperature clines) and
size, has been widely adopted (West, Brown & Enquist, short term (TSR responses during ontogeny).
1997; Savage et al., 2007). It should be noted, however, that As a more special case, Xia (1995) proposed an explanation
the role of a fractal distribution network within organisms for the increase in genome size through polyploidy under
only holds for metazoans, and other studies have proposed colder conditions. His idea was based on the fact that
the genome or cell size as the basic determinant of the growth in multicellular organisms or replication in unicellular
allometric exponent also in metazoans (Kozlowski et al., organisms involves a period of cell biosynthesis and a period
2003; Starostova et al., 2009; Maciak et al., 2011). of cell duplication, which are dependent on enzyme kinetics.
Increased absolute metabolic rate with increasing body Thus, an increase in the copy-number of genes at low
size may have implications for arguments both supporting temperature may offset the drawbacks of large cells by
and contrasting the general TSR. If supply of resources increasing the rate of biosynthesis.
(carrying capacity) is fairly constant, increase in absolute Interestingly, this optimization-of-biosynthesis theory
metabolic activity due to increasing temperature has to seems consistent with the work of Woods et al. (2003)
be balanced by decreasing individual mass and/or lower who found that cold-acclimated ectotherms contained higher
population density at equilibrium (see Daufresne et al., cell-specific levels of phosphorus (P) and rRNA than warm-
2009 and equation 9 from Brown et al., 2004). However, exposed conspecifics. This effect was interpreted as a reduced
under severe constraints of constantly limiting resource, food efficiency of protein synthesis at low temperatures, i.e. a
availability may be insufficient to support large animals higher level of ribosomes per unit protein produced at

Biological Reviews 88 (2013) 476–489 © 2012 The Authors. Biological Reviews © 2012 Cambridge Philosophical Society
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484 D. O. Hessen and others

low temperatures. Consistent with this hypothesis, Elser cool growth seasons selection may favour smaller genome
et al. (2000) found that body growth rate and P-content of and cell size to improve the thermal efficiency of growth rate.
individuals of the Daphnia pulex species complex were higher Since reduced cell size in itself may lead to reduced body size,
in Arctic water bodies compared to temperate lakes. The this may further strengthen selection for converse Bergmann
studies of Woods et al. (2003) and Elser et al. (2000) refer responses.
to a fundamentally different mechanism than that studied Thus, increasing time limitation towards colder areas may
by Xia (1995), but both systems appear shaped by the completely mask any effects of a temperature-dependent
same underlying demand to improve thermal efficiency in TSR. The overall consequences of both mechanisms will
metabolism and growth as an aspect of adaptation to low very much depend on the severity of time limitation. This
temperatures (Clarke, 1991, 2003; Birkemoe & Leinaas, is expected to be most pronounced in species with fixed
2001; Yamahira & Conover, 2002). It is worth mentioning (in particular annual) life cycles in terrestrial and freshwater
that increased ribosome copy number per cell may require habitats.
cytoplasm expansions and thus promote enlarged cell size. In species with a flexible life cycle, e.g. changing between
annual to 2- and even 3-year life cycles, one may observe
a saw-tooth-shaped pattern in body size towards colder
environments, reflecting gradual and more sudden shifts
V. ALTERNATIVE EVOLUTIONARY DRIVERS
in time constraints (Mousseau & Roff, 1989). This means
that within the range of one life-cycle pattern, increasing
In the previous section we mainly focused on the role of time stress with reducing temperature results in a gradual
temperature as a direct driver of change in genome or cell reduction of body size. But when the species adds another
size. This is unproblematic when referring to the TSR, year to its life cycle in even colder environments, time
which represents phenotypic responses to developmental stress becomes more relaxed and body size increases again.
temperature, as observed under controlled experimental Actually, in this situation, there is likely selection for
conditions (Angilletta et al., 2004). However, causations increasing size and thus fecundity, to compensate for costs of
for size clines along climate-related geographic gradients extending the life cycle. In species with multiple generations
may involve both phenotypic plasticity and long-term per year, or living in areas with little seasonality, time stress
evolutionary adaptations in body size, both of which towards colder areas appears less important, and change in
may reflect thermal responses as well as effects of other body size is more likely to follow a Bergmann cline (see e.g.
confounding factors. This complexity of causations makes it Chown & Klok, 2003).
hard to disentangle the underlying mechanisms, and thus any Compared to terrestrial and even freshwater habitats,
geographic clines along climate gradients should be judged high-latitude marine environments show very small seasonal
with caution. Confounding effects may relate more or less variations in temperature and the organisms are in general
directly to temperature, such as the heat sum available during active throughout the year. Consequently, predictions for
a growth season affecting time constraints on a life cycle, but temperature responses of organisms in the different systems
also may include factors that are independent of temperature, differ correspondingly, with Bergmann clines expected to
such as nutrient and light conditions, food availability and be most pronounced in cold marine waters. In fact,
size-selective predation, which all may vary along climate and especially among invertebrates at high latitudes,
gradients. body size may take the form of gigantism compared to
temperate relatives (Timoteev, 2001; Rees et al., 2007, 2008).
(1) Life-cycle effects and inversed TSR Interestingly, this gigantism in body size is also accompanied
by gigantism in genome size.
An increasing number of studies has shown distinct deviations This means that predictions for temperature responses will
from ‘Bergmann clines’ and even converse trends (Mousseau, differ between marine, terrestrial, and freshwater habitats.
1997; Karl & Fisher, 2008). The latter (called ‘converse Increasing temperature will generate reduced cell and body
Bergmann clines’) have mostly been studied in insects, such size in marine systems, while most likely generating increased
as grasshoppers (Mousseau, 1997), crickets (Mousseau & size in terrestrial or freshwater species with annual life
Roff, 1989), butterflies (Nylin & Svärd, 1991) and beetles cycles. For perennial, terrestrial species the temperature
(Chown & Klok, 2003), in environments where the length effect is more obscure, since these species will still have to
and temperature (heat sum) of the growth season is clearly maintain a high growth rate to cope with the short growing
correlated with the general temperature conditions. Notably, season.
fixed life-cycle patterns with specific overwintering stages
may, towards higher altitudes or latitudes, experience an
(2) Nutrition and diffusion
increasing pressure on growth rate to complete vital life-
cycle stages within a brief time window. These constraints We have argued that the same TSRs in principle may hold
may impose selection pressures that run counter to the for both protists and metazoans. To some extent this holds
general TSR, most evidently because smaller adult body size also for gas exchange, while autotroph and heterotroph
would reduce the heat sum needed to reach sufficient body protists and metazoans clearly differ with respect to nutrient
mass. However, it is also possible that in areas with short, uptake or intake. In both groups, gas exchange and nutrient

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Genome size and temperature in ectotherms 485

acquisition may act as confounding factors with temperature. (3) Predation

In unicellular osmotrophs, availability of dissolved gases (O2
Predation may work both ways, with large size being
and CO2 ) and nutrients may cause cell-size changes both at
beneficial for prey subject to small and non-selective
the species and community level. Gas exchange will be more
predation (e.g. Thingstad et al., 2005; Kaartvedt, 2008),
efficient in smaller cells with higher surface-to-volume ratios,
while size-selective or visual large predators such as fish
and since solubility of gases decreases with temperature,
provide a strong selection for small body size in metazoans.
temperature and gas exchange could act in concert since
Mesopelagic fishes represent a key functional group of visual
increasing temperature per se may decrease the maximum size
predators in most oceans, but are sparse in Arctic waters,
of a cell even under oxygen saturation (e.g. Moran & Woods,
partly reflecting the low-light regime. This could contribute
2010). There is a consistent increase in metabolic oxygen
to the prevalence of large-bodied invertebrates in these areas,
demands with temperature across taxa of marine ectotherms such as the large arctic Calanus species (Kaartvedt, 2008). It
(Clarke, 2003). This may imply selection for smaller species is therefore important to consider that there are alternative
at high temperatures, but also explain the gigantism of many explanations for body-size changes along temperature clines,
polar taxa (Chapelle & Peck, 1999) as well as diversity and and to design experimental studies on the temperature effect
size patterns among aquatic ectotherms (Verbek et al., 2011). per se.
While temperature regulation has been advocated as a deter-
minant of maximum and minimum body size in endotherms
(i.e. problems with heat loss in large animals, and heat (4) Effect of population size
retention in small), so gas exchange has been linked to at least Population-level effects may also have a direct bearing on
maximum size of invertebrates, where historic shifts in O2 genome size. In the absence of strong counter-selective
concentrations seem to match invertebrate size and in fact forces, there is an inherent tendency of non-coding DNA
may have been a key evolutionary driver (Berner, Vanden- to accumulate over generations (Lynch, 2007). This would
Brooks & Ward, 2007). Reduced levels of O2 have also been be a non-adaptive consequence of ‘selfish’ replicators,
predicted to cause decreased size in marine fishes worldwide which in principle is costly to the organism in terms of
(Cheung et al., 2012). Thus, temperature-related determi- increased mutation rate, material cost related to DNA itself
nants of O2 concentrations, especially in aquatic habitats, (Hessen et al., 2010) or metabolic costs related to large cells,
may be a regulator of size that deserves more attention. that at some point would counter-select further genome
Along the same lines of reasoning, cell volume is also expansion. Assuming that accumulation of transposons
a major determinant of nutrient uptake. Small cells have also induces an increased burden of mutations, large
generally higher uptake affinities for nutrients compared populations will more effectively counteract transposon
with larger cells owing to their higher surface area to proliferation compared with small ones (Lynch, 2007).
volume ratio (Tambi et al., 2009). This is especially true However, the extent to which this might have relevance for
for marine areas, where cold upwelling regions typically are the occurrence of Bergmann clines depends on the likelihood
more nutrient rich than warm areas, which could promote of species having population sizes that decrease towards cold
larger cells in such upwelled waters. Phytoplankton-size environments.
shifts both in marine waters (Gasol, del Giorgio & Duarte, The above sections provide by no means an exhaustive
1997) and lakes (del Giorgio & Gasol, 1995) have been list of potential confounding factors that could affect body,
attributed to nutrient gradients, and numerous experiments cell, or genome size along thermal or geographical clines,
have demonstrated higher nutrient affinity in small cells although they provide examples that call for some caution
due to large surface area to volume ratios (Finkel et al., when interpreting climate-correlated geographic clines as
2007). A survey of a large number of lakes suggests that temperature responses, important when applying such
nutrients override the effects of temperature on cell size (R. theories within a predictive framework. It is also interesting
Ptachnik, H. Hillebrand, T. Andersen & D. O. Hessen, in to note that different environmental factors may have
preparation), perhaps reflecting a wider range in nutrients different phenotypic effects on cell size and number. While
than temperature in the surveyed lakes. Also for metazoans, temperature seems mainly to affect cell size, food or nutrients
claimed temperature effects on body size could in fact be have a strong impact on cell number, a pattern shared by
a nutrient effect in disguise (Yom-Tov & Geffen, 2011). insects and plants (Arendt, 2007).
Cold environments are often characterized by brief periods
of spring blooms, followed by long periods of low food
availability that benefit larger organisms with greater energy-
storage capacities. VI. GLOBAL-CHANGE IMPLICATIONS
Finally, it has been suggested that P-limitation in itself
may promote downsizing of genomes since this would pose The flip side of the traditional focus on increased size at low
a selective pressure for reducing the allocation of P to temperature is the potential evolution or shift towards smaller
non-coding elements, and eventually a reallocation from cells or genomes with elevated temperatures. There is recent
DNA to RNA (Hessen, Ventura & Elser, 2008; Hessen evidence from aquatic ecosystems that such size reductions
et al., 2010). indeed do occur for a wide range of aquatic organisms

Biological Reviews 88 (2013) 476–489 © 2012 The Authors. Biological Reviews © 2012 Cambridge Philosophical Society
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486 D. O. Hessen and others

(Daufresne et al., 2009), although primarily focusing on distinct patterns: a decrease in the size-at-age only tested for
phytoplankton (Falkowski & Oliver, 2007; Finkel et al., 2007; fish of less than 1 year old and an increase in the proportion of
Winder, Reuter & Schladow, 2009; Morán et al., 2010; juveniles i.e. less than 1-year-old fish. This again suggests that
Sarmento et al., 2010). Consistent patterns with smaller responses to changes in thermal environment are complex
cells in warmer waters was found in the North Atlantic and play out at different biological scales by involving
Ocean, but this was primarily credited to a larger fraction processes related to both phenotypic and life-history-trait
of picophytoplankton with elevated temperatures (Morán variability. In support of this, Ohlberger et al. (2011) predicted
et al., 2010), and, as noted by Yvon-Durocher et al. (2011), decreasing mean size in fish in response to increasing
such gradient effects are hard to interpret due to potential temperature at the population level as a result of changes in
confounding effects of nutrients and temperature. size composition, and recently Cheung et al. (2012) predicted
There are several routes to shifts in phytoplankton size a potential shrinking of 14–25% in maximum body size
composition, and these are not mutually exclusive. Adding in marine fish under a high-CO2 -emission scenario. From
to a number of marine surveys that are supportive of a strong this viewpoint, the direct ecosystem responses to temperature
temperature–cell size coupling, Winder et al. (2009) found a and coupled temperature-nutrient-O2 driven shifts in the size
corresponding response in a long-term study of Lake Tahoe. structure of ecosystems should be one of the key motivators
Additionally there is strong evidence that experimentally to gain further insights into TSR responses (Sheridan &
induced warming may shift the community composition Bickford, 2011).
towards smaller cells in lake enclosures (Yvon-Durocher
et al., 2011).
Other studies have questioned the universality of these VII. FUTURE DIRECTIONS
findings. For example, Byllaardt & Cyr (2011) did not
record any temperature-related changes in size of benthic While there are many striking correlations between size and
diatoms within sites of a lake, in fact often the converse temperature, the causal relationships are still rather unclear
was observed. They did, however, record a distinct site- and different mechanisms may be operating in different
related pattern, pointing to other drivers such as nutrient organisms, in different ecosystems and at different timescales.
concentrations. Temperature and nutrient effects are not Indeed, evolutionary drivers may not be the same at the
mutually exclusive, however, and it is reasonable to assume genomic (or cellular) level and the body-size level, and our
that at fixed or nearly stable nutrient concentrations, effects of main argument here has been that more research should
temperature would be more manifest. One may also expect be devoted to the genomic responses. This should include
that the nutrient effect would be most prevalent under both evolutionary adaptations along temperature gradients
severe nutrient limitation. The common coupling between as well as ontogenetic responses and ‘passive’ responses in
temperature and nutrient levels, i.e. the highest nutrient terms of intron accumulation versus ‘active’ responses by gene
concentrations are often found in cold waters with upwelling duplications. Reduced cell size will pose pressure for genome
or at least weak stratification and more turbulent mixing, streamlining, causing increased metabolic rates, increased
could cause apparent temperature effects to be credited cell division rates, elevated growth rates, increased grazing
to nutrient responses (cf. Agawin, Duarte & Agusti, 2000; rates, increased trophic efficiency and reduced standing stock
Yvon-Durocher et al., 2011). Yvon-Durocher et al. (2011) of autotrophs. The latter effect will also be promoted by
thus applied outdoor mesocosms to isolate the effects of increased thermal stability and reduced access to nutrients
temperature, but their results still showed that increasing in the euphotic zone.
temperature yielded smaller cells. This again reduced the There is thus a need for more ‘common garden’
phytoplankton to zooplankton biomass ratio since small cells experiments where conspecific populations or closely related
were subject to heavier grazing pressure and thus the standing species from contrasting thermal environments are raised at
stock was reduced, but higher phytoplankton growth rate was different temperatures to disentangle phenotypic plasticity
observed due to high nutrient cycling from zooplankton. No versus genetic-based differences in body size. Importantly,
doubt there are several reasons to expect reduced cell size since a phenotypic response to thermal variation in itself
and body size with elevated temperatures. In particular may be an important adaptation, it is likely to be affected
for marine systems, several mechanisms may interact since by selection (Yamahira & Conover, 2002; Chown & Gaston,
both warmer waters and reduced nutrients due to increased 2010). Thus, micro-evolution may not just lead to differences
thermal stability will cause reduced size of protists. Similarly in trait means between conspecific populations, but also in
increased temperature will be accompanied by reduced how the different populations are affected by changes in
concentrations of O2 which both would favour smaller cells temperature; i.e. genotype × environment interaction (e.g.
and organisms (Cheung et al., 2012). Mousseau & Roff, 1989).
Few studies have really addressed intraspecific responses Clearly, a deeper understanding of the genome responses
to warming, although the studies of Daufresne et al. (2009) is warranted. For example deep sequencing should be used
showed that mean size at the population scale tends to to look for structural changes in coding versus non-coding
decrease with global warming in different fish populations. regions. A closer look also is warranted into the prevalence
This decrease in mean body size was mainly due to two and effects of somatic endopolyploidy with ontogeny and

Biological Reviews 88 (2013) 476–489 © 2012 The Authors. Biological Reviews © 2012 Cambridge Philosophical Society
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Genome size and temperature in ectotherms 487

the incidence of polyploidy between related species along (polyploidy in the case of full chromosomal duplications)
thermal gradients. All of these would shed light on causal or accumulation of non-coding elements (introns) expanding
effects. Also, the phylogenetic effects would need further the haploid (or diploid) genome size. Both these events
scrutiny. While phylogeny clearly is important for genome- seem especially common under low temperatures, generally
and cell-size patterns, these attributes could themselves causing enlargement of cells and eventually body size. Thus,
contribute to speciation. A striking feature of some taxa genome size increase at low temperature may reflect a passive
adhering to temperature-size patterns is their morphological response of accumulation of ‘selfish DNA’, e.g. by transposon
similarity despite strong differences in body size. In cases proliferation simply because there is a low counter-selective
where this reflects genome duplication events or an expansion pressure at low growth rate (or low population density).
of genome size due to proliferation of non-coding elements, Alternatively, it may reflect gene duplication to enhance
this could represent a fast route to speciation. This could enzyme expression or protein synthesis at low temperature,
be due to both changes in body proportions and life-cycle i.e. an active and fitness-promoting response at the organism
mismatch in reproductive periods and directly by mismatch level. These two responses are not mutually exclusive, but
in chromosome size during zygote formation. can be separated by genetic screening.
In contrast to the climate clines, the TSR reflects (4) We here offer a novel perspective on the temperature-
phenotypic plasticity in the form of thermal reaction norms size rules from a ‘bottom-up’ perspective: how temperature
for body size, which can only be studied experimentally by may induce changes in genome size, and thus implicitly
controlled manipulation of temperature during development. in cell size and body size of metazoans. We believe this
The current literature gives the impression that the TSR is is a general trait both for protists and many invertebrates,
more general than Bergmann clines; i.e. that a phenotypic although the responses may differ in different environments.
negative relationship between body size and developmental In marine ecosystems, low temperature coincides with large
temperature is more common than the tendency for genomes and large cells (and large body size for metazoans),
populations to become larger in colder environments. while it may work in an opposite direction for terrestrial
However, this impression may be biased by the fact that insect and freshwater invertebrates. This has major ecological
species showing Bergmann clines generally are smaller, with and evolutionary implications for growth, metabolism and
shorter generation times than species following the converse evolution.
Bergmann cline. Consequently, the former group is easier to (5) If temperature-driven changes in genome size, either
keep in culture and may be overrepresented in experiments via polyploidy or accumulation of non-coding elements
studying the effects of developmental temperature. such as transposons, result in significant differences between
Since the issues covered herein literally deal with the populations in body size, allometry or life-cycle events like
core of life, we believe that further insights into the various mating season, they could represent a fast route to speciation.
mechanistic drivers for changes in genome, cell and body
size, as well as the relationships among these metrics, will
reveal fundamental aspects of evolutionary principles related IX. ACKNOWLEDGEMENTS
to allometry and leave us better equipped to predict effects at
all levels from cells to ecosystems as a consequence of global This project received grants from the Norwegian Research
warming. Council ‘Genome’ (project no. 196468) to D. O. H. We
acknowledge Jan Ohlberger and Steven Chown for valuable
comments and inputs to drafts of this manuscript, and three
VIII. CONCLUSIONS anonymous reviewers for their most thorough and helpful
comments.
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(Received 5 July 2012; revised 8 November 2012; accepted 20 November 2012; published online 18 December 2012)

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