Temperature gradient affects differentiation of gene ...

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5%–15% of volume per year (Kozhova & Izmest'eva, 1998; Verbolov,. 1996). ...... Nogales, & Downing, 2000; Pucciarelli et al., 2009; Tartaglia & Shain,.

Received: 17 November 2017

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Revised: 20 March 2018

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Accepted: 27 March 2018

DOI: 10.1111/mec.14704

ORIGINAL ARTICLE

Temperature gradient affects differentiation of gene expression and SNP allele frequencies in the dominant Lake Baikal zooplankton species Larry L. Bowman1 | Elizaveta S. Kondrateva2,3 | Maxim A. Timofeyev4 | Lev Y. Yampolsky1 1 Department of Biological Sciences, East Tennessee State University, Johnson City, Tennessee

Abstract Local adaptation and phenotypic plasticity are main mechanisms of organisms’ resili-

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Institute of Biology, Irkutsk State University, Irkutsk, Russia

ence in changing environments. Both are affected by gene flow and are expected to

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be weak in zooplankton populations inhabiting large continuous water bodies and

Baikal Research Centre, Irkutsk, Russia

Siberian Institute of Plant Physiology and Biochemistry SB RAS, Irkutsk, Russia

strongly affected by currents. Lake Baikal, the deepest and one of the coldest lakes

Correspondence Lev Y. Yampolsky, Department of Biological Sciences, East Tennessee State University, Johnson City, TN. Email: [email protected]

exposing Baikal’s zooplankton to novel selective pressures. We obtained a partial

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Present address Larry L. Bowman, Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut.

on Earth, experienced epilimnion temperature increase during the last 100 years, transcriptome of Epischura baikalensis (Copepoda: Calanoida), the dominant component of Baikal’s zooplankton, and estimated SNP allele frequencies and transcript abundances in samples from regions of Baikal that differ in multiyear average surface temperatures. The strongest signal in both SNP and transcript abundance differentiation is the SW-NE gradient along the 600+ km long axis of the lake, suggesting isolation by distance. SNP differentiation is stronger for nonsynonymous than synonymous SNPs and is paralleled by differential survival during a laboratory

Funding information National Science Foundation, USA, Grant/ Award Number: 1136710, 0742364; Russian Science Foundation, Grant/Award Number: 17-14-01063

exposure to increased temperature, indicating directional selection operating on the temperature gradient. Transcript abundance, generally collinear with the SNP differentiation, shows samples from the warmest, less deep location clustering together with the southernmost samples. Differential expression is more frequent among transcripts orthologous to candidate thermal response genes previously identified in model arthropods, including genes encoding cytoskeleton proteins, heat-shock proteins, proteases, enzymes of central energy metabolism, lipid and antioxidant pathways. We conclude that the pivotal endemic zooplankton species in Lake Baikal exists under temperature-mediated selection and possesses both genetic variation and plasticity to respond to novel temperature-related environmental pressures. KEYWORDS

Baikal, differential expression, Epischura, SNPs, temperature, zooplankton

1 | INTRODUCTION

Lenz, 2015; Pavey, Bernatchez, Aubin-Horth, & Landry, 2012). The advent of NextGen sequencing made it possible to analyse, on a

Understanding how organisms adapt to their local environment is

genome- or at least transcriptome-wide scale, both fundamental

one of the key goals in molecular ecology (Bedford & Hartl, 2009;

mechanisms of surviving in an environment that changes in time and

Chen et al., 2012; Dayan, Crawford, & Oleksiak, 2015; Fraser, 2013;

ry et al., 2014; Dayan et al., 2015; space: local adaptation (Csille

Molecular Ecology. 2018;1–16.

wileyonlinelibrary.com/journal/mec

© 2018 John Wiley & Sons Ltd

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Eckert et al., 2015; Fraser, 2013; Lavington et al., 2014; Simonson

5%–15% of volume per year (Kozhova & Izmest’eva, 1998; Verbolov,

et al., 2010) and adaptive phenotypic plasticity (Bedford & Hartl,

1996). The South basin historically has been the warmest of the

€ tterer, 2015; Dayan et al., 2015; 2009; Chen, Nolte, & Schlo

three, with epilimnion temperatures 1–2°C (Shimaraev, Verbolov,

Klumpen et al., 2017; Rohlfs, Harrigan, & Nielsen, 2014; Schwerin

Granin, & Sherstyankin, 1994) higher than the Central and North

et al., 2009; Yampolsky, Zeng et al., 2014). These two responses to

basins during summer months. Additionally, Baikal’s largest island, I.

environment—differentiation with respect to heritable changes and

Olkhon, is separated from the western shore by a broad strait called

nonheritable physiological and biochemical changes—are often diffi-

Maloe More; this region of the lake is shallow in comparison with

cult to untangle in the field and, in case of differential mortality,

other open parts of Baikal (only up to 200 m), but has a similar ther-

even in laboratory studies.

mal regime to open Baikal, as it shares circulation with the North

In the last few years, we have seen an explosion of previously

basin (Kozhova & Izmest’eva, 1998). However, the southernmost,

impossible studies addressing the degree and functionality of these

shallow end of the Maloe More strait is regularly experiencing much

two mechanisms in a variety of species along a variety of environ-

higher surface temperatures than open Baikal (Kozhova & Izmes-

mental gradients. While data describing differential gene expression

t’eva, 1998; Shimaraev et al., 2002).

along environmental gradients are abundant (Bedford & Hartl, 2009;

The South basin average surface water temperature has been

Clark et al., 2017; Gautier, 2015; Zhao, Wit, Svetec, & Begun, 2015),

steadily rising during the last century, showing over 1°C increase

it is not always clear if such differentiation has a genetic basis, that

in 60 years (Hampton et al., 2008; Shimaraev et al., 2002). The

is, if it is accompanied by local differentiation and if it does, whether

Central and North basins have shown a similar increase in average

the forces that shape differentiation and differential expression are

epilimnion temperatures in more recent data (Izmesteva et al.,

parallel or orthogonal to each other (Dayan et al., 2015). Further-

2016), while the South basin appeared not to warm up any further

more, it is not clear how much lists of candidate genes reported by

in the last 20 years. There are no systematic data on temperature

different studies agree with each other and how applicable findings

extremes, but anecdotal evidence suggests increased frequency of

obtained using model organisms are for other biological situations

episodes of abnormally high surface temperatures (15–18°C), par-

(Clark et al., 2017); the need to consolidate ecological genomics

ticularly in the South basin in the southernmost end of Maloe

results across different organisms and across functional groups of

More.

genes has been long identified (Pavey et al., 2012).

While an increase of about 1°C over half a century might not

Recent estimates of global climate change suggest that surface

appear to be a radical change, such changes are, arguably, signifi-

temperatures increased by about 1°C over the last 100 years (IPCC,

cant relative to Baikal’s endemics fauna narrow thermal tolerance

2014). Lake Baikal in Siberia, Russia, the deepest, the most volumi-

range. Such endemic species, including a pivotal zooplankter Epis-

nous, the oldest and one of the coldest lakes on Earth, appears to

chura baikalensis (Copepoda: Calanoida), essentially have not been

be slightly ahead of this trend, both in terms of absolute and relative

exposed to temperatures significantly above 4°C throughout their

temperature changes (up to 2°C surface temperature increase over

evolutionary history at least since pre-Pleistocene time or since

the last ~50 years; Hampton et al., 2008; Izmesteva et al., 2016; Shi-

their colonization of Baikal. The only exception from this stenother-

maraev & Domysheva, 2013). Baikal stretches over 600 km from

mic environment is the exposure to higher temperatures during

SW to NE, and the opposite ends of the lake are located in rather

diurnal vertical migration (DVM) that E. baikalensis exhibit in order

different climates. The SW end experiences the relatively warm sum-

to reach phytoplankton-rich surface waters at night. As surface (but

mers of south Siberia with average yearly temperatures within the

not hypolimnion) temperatures increase, so does the strength of

5° to 0°C range and with 100–120 days of average daily tempera-

stratification potentially exposing Baikal’s zooplankton to a warmer

ture above +10°C per year. Meanwhile, the NE end of the lake is

epilimnion (Hampton, Gray, Izmest’eva, Moore, & Ozersky, 2014).

exposed to the very cold winter and mild summers of central-east

The DVM feeding requirement is not absolute, as a deep chloro-

Siberia with average yearly temperatures below 5°C and with

phyll maximum exists in Baikal and is often observed immediately

0.1). Filtering by orthologous group (OG) leaves in the enrichment analysis only those transcripts that are members of orthologous groups previously identified as candidate genes for thermal adaptation by seven or more studies (see text)

include (Supporting information Table S4) heat-shock proteins (eight

transcript abundance show paralogs of glutathione S-transferases,

transcripts from three OGs upregulated in warmer areas, additionally

superoxide dismutase, cathepsin protease, beta subunit of Na/K-

two transcripts possess outlier SNPs); glutathione metabolism

transporting ATPase, among others.

enzymes (two transcripts up- and two downregulated in warmer areas); haemocyanins (four transcripts upregulated in warmer areas); cytochromes (two transcripts upregulated in warmer areas); as well as numerous proteases (five transcripts from three OGs upregulated and two others downregulated in warmer areas). Many of these instances of differential expression along the thermal gradient in the

4 | DISCUSSION 4.1 | SNP allele frequencies and gene expression levels are differentiated across Baikal

field are paralleled by those observed in the laboratory, although

Gradual warming of the epilimnion in several parts of Lake Baikal

there are several notable exceptions, in particular among actins and

constitutes an environmental pressure on the lake zooplankton,

tropomyosins, all of which are downregulated in the laboratory sam-

resulting in both phenotypic plasticity and, potentially, response to

ples. Numerous OGs show bidirectional changes in paralogs’ expres-

selection. Indeed, we find that the SW-to-NE main axis of the lake

sion with respect to thermal conditions. These include several

and the parallel long-term August–September surface temperature

families of structural proteins (actins, four transcripts up- and four

gradient are the major determinants of both SNP allele frequencies

downregulated; myosin light chains, three up- and four downregu-

and transcript abundance. Thus, Epischura baikalensis possesses both

lated; tropomyosins, three up- and three downregulated; and a-tubu-

the regulatory mechanisms and genetic variability allowing physiolog-

lins, one up- and six downregulated). Similarly, opposite changes in

ical acclimation and response to selection, respectively, when facing

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elevated temperatures. We hypothesize that such mechanisms exist

Correlations with longitude and latitude suggest that the differ-

because they allow acclimation to higher temperatures during diurnal

entiation of SNPs along the SW-to-NE axis is largely based on isola-

vertical migration (DVM) into the warmer epilimnion and, therefore,

tion by distance, as it is consistent with major current circulations

that further warming of Baikal’s epilimnion is more likely to cause an

within the lake, namely with the existence of partially isolated circu-

evolutionary response in this pivotal pelagic species than radical

lations in the South, Central and Northern basins, the latter encom-

changes in abundance and/or extinction. As is common in field stud-

passing also the Maloe More strait (Verbolov, 1996). Yet, each of

ies, we are unable to differentiate between heritable selective

the three main Baikal basins exchanges 5%–15% of water volume

responses and transcriptional phenotypic plasticity. Even when dif-

per year with the neighbouring basins (Verbolov, 1996). Typical cur-

ferential expression is analysed in a set of genes with no differenti-

rent velocities (2–4 cm/s, i.e., 1.7–3.4 km/day or 300–600 km per

ated SNPs, DE can still be caused by heritable differences in cis- or

season; Verbolov, 1996) imply that an individual copepod could tra-

trans-regulatory regions not covered by our transcriptome-based

vel the entire length of Baikal with little possibility for active hori-

data. A common-garden experiment with Epischura from different

zontal movement within its lifespan (at least in the summer

parts of the lake would be needed to differentiate between the two

generation when currents are strong). Thus, the among-basin differ-

mechanisms.

entiation cannot be maintained without a strong selection for local

It should be noted that the above results are also limited to tran-

adaptation. It should be noted that much of this water exchange is

scripts present in high abundance in adult Epischura during the spring

limited to surface waters (top 50–100 m; Verbolov, 1996), inhabited

reproduction period and therefore represented in our partial refer-

by a significant portion of E. baikalensis population (Afanasyeva,

ence transcriptome. Therefore, they do not include any potential sig-

1998). This means that the magnitude of horizontal gene flow

nals present in genes active during embryonic development, in

depends on the existence of vertical genetic differentiation, often

nauplial and early copepodite stages or in low-abundance transcripts

observed in lake zooplankton (Seda, Kolarova, Petrusek, & Machacek,

missed by the de novo reference transcriptome assembly. Further-

2007) and suggested by the differentiation between surface and

more, the above analyses of SNP differentiation in paralogs are lim-

deep samples of the only station for which such data are available in

ited to paralogs with sufficient sequence divergence allowing correct

this study (Figure 2a, samples SB3D and SB3S). If the differentiation

assembly and mapping, while very young duplicated genes, though

between the deep (nonmigrating) and shallow (showing DVM) popu-

perhaps the most interesting in the context of selective response,

lations of E. baikalenis is real (previously shown in other calanoids in

are indistinguishable from alleles and thus escape this analysis.

Schizas, Dahms, Ricaurte, & Hwang, 2014), the observed geographic

Finally, there are probably paralogs with “twilight-zone” divergence

differentiation may reflect relative abundance of these populations

level that can, given they also show differential expression, create a

across the parts of the lake with different depths and degree of

spurious apparent differentiation of SNP alleles. The transcript-level

stratification. Functional genomics of the differences between deep

filters we employed, in particular, the removal of transcripts with

and shallow samples will be reported elsewhere (L. Y. Yampolsky, in

paralogs with >90% identity over more than 90 bp, likely amelio-

preparation).

rated this problem to some extent.

SNP differentiation results offer several lines of evidence sup-

Correlations between geographic location (e.g., latitude) and

porting the local adaptation hypothesis. First, the differentiation

allele frequencies (Lavington et al., 2014) at temperature-related

along the first principal component deviates from the SW-to-NE axis

loci or temperature-related phenotypes (e.g., Yampolsky, Schaer, &

consistent with selection operating in the warmest parts of the lake:

Ebert, 2014) are frequent when gene flow is expected to be low.

one of the two Maloe More samples, MM2, that is, the one from

High levels of gene flow set the limits to local adaptation (Lenor-

the warmest and shallowest location, shows disproportionally “south-

mand, 2002), unless selection is strong and operates on few large-

western” allele frequencies (Figure 2). This pattern is paralleled by

effect alleles (Yeaman & Otto, 2011; Yeaman & Whitlock, 2011).

differential survival during a laboratory acclimation to increased tem-

Indeed, despite high levels of gene flow facilitated by currents in

peratures (Figure 2f). Second, SNP differentiation (both the differen-

marine and large lake environments, large-scale differentiation has

tiation of stations within regions and regions within the lake) is

been observed in zooplankton populations, provided that a suffi-

stronger for nonsynonymous than synonymous SNPs (Figure 1).

cient number of SNP loci are analysed (Blanco-Bercial & Bucklin,

Finally, SNP differentiation is collinear with the variation in transcript

2016). Baikal’s E. baikalensis seems to be no exception: a previous

abundance in a nonoverlapping set of transcripts (Figure 3) that are

mtDNA-based study did not reveal any differentiation among Bai-

enriched in orthologs of genes previously repeatedly identified as

kal’s major basins (Zaidikov, Maior, Sukhanova, Kirilchik, & Nau-

candidates for adaptive thermal response (Supporting information

mova, 2015), while in the present study, we observe such

Figure S10). On the other hand, transcripts with outlier SNP them-

differentiation at hundreds of (presumably nuclear) SNPs, both

selves do not show any enrichment with previously identified candi-

among stations within the same basin and among basins. The inter-

date orthologs (Supporting information Figure S10C), which can be

play between local adaptation and migration is believed to be the

readily explained by a high frequency of false positives due to link-

likely cause for genetic differentiation within lakes or marine envi-

age to the actual loci under selection.

ronments despite high gene flow (Blanco-Bercial & Bucklin, 2016; Vaillant et al., 2013).

Similarly, in the analysis of a subset of transcripts with both outlier SNPs and significant DE, a strong isolation by distance is

BOWMAN

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observed, with DE generally being similar in genetically more similar

as the change from never being exposed to temperatures above 4°C

populations (Supporting information Figures S6 and S7). However, in

during the last glaciation, to occasional such exposures during the last

concordance with similar findings by Dayan et al. (2015), there were

10–12 Ky and to, likely, more frequent such exposures, in particular in

deviations from this pattern with some of the populations showing

South Baikal and the southernmost end of Maloe More, during the last

expression profiles similar to other populations sampled from war-

100 years. No data on the frequency of such exposures exist, but

mer areas of Baikal and not to those with the most similar SNP allele

anecdotal evidence suggests the regular occurrence of surface tem-

frequencies. This indicates that, in genes that demonstrate both

peratures that once were considered exceptional.

adaptive differences and phenotypic plasticity (Dayan et al., 2015), DE and SNP variation act on different gradients.

4.4 | Functional genomics of possible response to thermal challenges in E. baikalensis

4.2 | Laboratory exposure parallels differentiation along the thermal gradient in Baikal

What kind of functional response to the current thermal environ-

The results of the laboratory temperature exposure experiment were

lier SNPs with allele frequencies correlated with the first two

in general agreement with the data from the thermal gradient in nat-

principal components and thus showing the NE-SW differentiation

ure. Just as in case of field samples data, we cannot distinguish

along the main axis of the lake or showing a significant DE along this

between plastic (differential expression) and selective (differential

axis encode for enzymes participating in central energy metabolism,

survival) responses in this experiment, particularly given elevated

including glycolytic and oxidative phosphorylation pathways (Sup-

mortality at higher temperature treatments. However, the results

porting information Figure S8). This is consistent with similar findings

support the hypothesis that both effects were observed, likely

for the latitudinal gradient in Drosophila (Lavington et al., 2014) and

affecting different sets of genes (Figure 3). Both the genes with a

for the North vs. South comparisons in Daphnia (Yampolsky, Zeng

significant DE (Figure 2c,g) and with SNP outliers (Figure 2f, Sup-

et al., 2014). However, in contrast with the Daphnia result, here we

porting information Figure S4) show a parallel trend in the laboratory

observe upregulation of subunits of DNA and RNA polymerases

experiment and field samples, supporting the hypothesis that tem-

(Supporting information Figure S8B) in E. baikalensis from warmer

perature is a major factor shaping plasticity and differentiation.

areas of Baikal, while Daphnia clones showed a massive downregula-

ment can we detect? A number of transcripts either containing out-

tion of transcripts related to transcription and DNA replication at

4.3 | Past and current selective pressures on Baikal zooplankton

higher temperatures (Yampolsky, Zeng et al., 2014). The observed opposite directions of DE (Supporting information Figure S8B) in at least some of the enzymes participating in a-linolenic acid metabo-

How novel are the current selective pressures relative to the evolu-

lism (downregulated in warmer areas) vs. linoleic and arachiodonic

tionary history of E. baikalenis in Baikal? How long Epischura has

acids metabolism (upregulated in warmer areas) are intriguing. If true,

existed in Baikal is unknown. The only estimate of divergence from

this may indicate a shift in availability of essential omega-3 and

the non-Baikal relatives is available from the internal transcribed

omega-6 polyunsaturated fatty acids at different temperatures, con-

spacer (ITS) and COI sequences from E. baikalensis and E. chankensis

sistent with the prediction obtained for a variety of phytoplankton

from the Far-East Lake Khanka (I. Zaidykov, unpublished data), show-

organisms (Hixson & Arts, 2016) and with a similar pattern of oppo-

ing, respectively, 5.9% and 19.3% divergence between the two species

site directionality of a-linolenic and linoleic acid accumulation

for the ITS and COI sequences, respectively. Biogeography-based cali-

observed in Daphnia (Martin-Creuzburg, Coggins, Ebert, & Yampol-

brations are difficult, and few of the necessary assumptions (Ho et al.,

sky, 2018).

2015) can be met for this comparison, but, as a very rough estimate,

The transcripts orthologous to candidate genes previously

one can use the calibration of Lee (2000) who estimated divergence

repeatedly identified by genomewide studies that showed upregula-

time among East Atlantic, West Atlantic and Pacific populations/cryp-

tion in the warmer areas of the lake and during elevated tempera-

tic species of Epischura’s marine relative Eurytemora affinis. She

ture exposure in the laboratory includes the usual and highly

observed a similar level of differentiation in COI sequences (~10%–

expected list of functionalities: cytoskeleton proteins, heat-sshock

25%) and was able to calibrate the divergence time using established

proteins, proteases and proteins involved in oxygen transport as well

16S calibration, with the same populations showing ~5% 16S diver-

as antioxidant and redox metabolism. This constitutes a different

gence, at approximately 5.1 My. Assuming that the same calibration is

approach from analysing transcript abundance and/or SNP differenti-

applicable to large lake freshwater Epischura and that E. chankensis is

ation ab initio to identify candidate genes. Instead, an a priori list of

not of Baikal origin, this gives us a very rough estimate of E. baikelenis

candidate genes is assembled (Jansen et al., 2017) and expected pat-

divergence from non-Baikal relatives at about 5 My. This suggests

terns of expression and differentiation are sought among orthologs

pre-Pleistocene origin of E. baikalensis, implying that it has survived

of such genes. While we are unable to identify previously entirely

repeated glaciations, including periods of long-term ice coverage last-

overlooked or organism-specific candidate genes using this approach,

ing possibly thousands of years (Karabanov et al., 2004). Thus, the

it is certain to be less prone to numerous false positives caused by

changes in the thermal environment for E. baikalensis can be described

higher priors. It is important that a single occurrence or a few

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ET AL.

occurrences of an orthologous group among candidate genes found

warmer areas of the lake is a copepod-specific paralog that differs

in model organism studies do not help to reduce such false positives:

from the ancestral crustacean a-tubulins by amino acid substitutions

it is repeated (in this analysis—over 8) independent findings that sig-

in the same areas (M-loop and adjacent a-helices) that contain amino

nal a significantly greater than expected agreement among studies

acid changes in cold-adapted fish (Detrich et al., 2000) and ciliates

and therefore positively identify a candidate orthologous group.

(Pucciarelli et al., 2009) and are known to play a role in tempera-

Such greater than expected agreement between this study and

ture-specific microtubule stability (L. Y. Yampolsky, in preparation).

genomewide studies in model organisms in terms of identifying tem-

Similarly, actins, myosins and tropomyosins have long been

perature response of orthologs with similar functionality is further

known to evolve according to temperatures and hydrostatic pres-

corroborated by gene- or function-specific biochemical and physio-

sures of organisms’ habitats to ensure thermodynamically plausible

logical results. Increased oxidative stress and/or measurable antioxi-

muscle filament assembly (Swezey & Somero, 1982) or to show plas-

dant

been

tic response to temperature (Johnston & Temple, 2002; Watabe,

demonstrated for a variety of aquatic organisms (Lesser, 2006;

2002). One may hypothesize that differential expression of eight

Tomanek, 2011), including marine calanoid copepods (Vehmaa et al.,

transcripts of actin-encoding and five myosin light chain-encoding

2013) and Lake Baikal amphipods (Axenov-Gribanov et al., 2016).

genes across Baikal’s basins may be related to differences in temper-

We believe that it is potentially important that different transcripts

ature or, alternatively, to differences in hydrostatic pressure experi-

of functionally similar key antioxidant pathway enzymes show oppo-

enced by populations of deep main basins vs. the shallower Maloe

site directions of DE changes, indicating possible ecological subfunc-

More strait. The observed differential expression and possible

tionalization (Colbourne et al., 2011). Specifically, two paralogs of

genetic differentiation of cytoskeleton-related transcripts are, there-

one of the glutathione S-transferase orthogoups are downregulated

fore, in agreement with similar results found in heat- or hypoxia-

along the cold-to-warm gradient, while a member of another glu-

related stress proteomics studies in a variety of aquatic poikilother-

tathione S-transferase orthogroup is upregulated; likewise out of

mic organisms including marine bivalves (Haslbeck, Franzmann,

two Cu-Zn-superoxide dismutase paralogs, one is down- and the

Weinfurtner, & Buchner, 2005), marine crabs (Garland, Stillman, &

other is upregulated along the thermal gradient (Supporting informa-

€ltz, & Tomanek, Tomanek, 2015), marine tunicates (Serafini, Hann, Ku

tion Table S4). The nature of such possible subfunctionalization is

2011) and freshwater fish (Chen, Cole, & Rees, 2013). Finally, the

unknown, but one may speculate that it may be based on either dif-

downregulation of numerous cuticle proteins in warmer areas of the

ferent functionality of paralogs (i.e., on specialization by metabolic

lake and in the laboratory experiment (Supporting information

pathways or cellular components) or on trade-offs between optimal

Table S4) is consistent with similar observations for their orthologs

performance at different temperatures (Genge et al., 2016; Hu, Lin,

in a parasitic copepod Lepeophtheirus salmonis larvae (Sutherland

Chi, & Charng, 2012).

et al., 2012;) and with the previously hypothesized role of cuticle

capacity

response

to

higher

temperatures

has

It is worth mentioning that, while heat-shock proteins are, predictably, uniformly upregulated in warmer parts of the lake, there is

proteins in swimming efficiency in Cyclops (Alcaraz & Strickler, 1988).

also an apparent bidirectionality of HSPs’ response to elevated temperature

in

a

laboratory

experiment

(Supporting

information

Table S4), consistent with a similar finding in laboratory temperature

5 | CONCLUSIONS

acclimation in Daphnia (Yampolsky, Zeng et al., 2014). Yet another functional group of proteins that show bidirectional changes along

Lake Baikal’s pivotal zooplankter, the endemic Epischura baikalensis,

the cold-to-warm axis are proteases, in particular serine proteases,

shows both significant differentiation of allele frequencies at SNP

€ lling which is, again, consistent with recent findings in Daphnia (Do

loci and significant differential transcript expression along the NE-to-

et al., 2016; Schwerin et al., 2009) and may, in addition to thermal

SW axis of the lake, despite a strong degree of admixture caused by

response, be a response to protease inhibitors produced by warm-

currents. These differences are concordant with each other and with

water phytoplankton (Schwarzenberger et al., 2012).

the geographic distribution of samples, indicating the role of isolation

Likewise, the finding that several orthologous groups showing

by distance. However, there are exceptions to geographic proximity’s

differential expression along the thermal gradient contain structural

effect on allele frequencies and transcript expression profiles—sam-

proteins of cytoskeleton is consistent with the previously described

ples from the warmest areas clustered together and not necessarily

thermal adaptation in cytoskeleton proteins of a striking variety of

with the geographically closest samples. This pattern is repeated

eukaryotes. In particular, a- and b-tubulins in cold-adapted fish,

when comparing field samples with samples exposed to elevated

annelids and ciliates show signatures of adaptation for efficient

temperatures in the laboratory, indicating selection favouring high

microtubule assembly at low temperatures (Detrich, Parker, Williams,

temperature tolerance. Functionalities of proteins showing a consis-

Nogales, & Downing, 2000; Pucciarelli et al., 2009; Tartaglia & Shain,

tent transcriptome response along the thermal gradient within Baikal

2008); differential expression of paralogs of tubulins plays a role in

include heat-shock proteins, proteases, key enzymes in antioxidant

cold acclimation in plants (Christov, Imai, & Blume, 2008; Farajalla &

pathways and several different cytoskeleton proteins including actins

Gulick, 2007) and Drosophila (Myachina, Bosshardt, Bischof, Kirsch-

and tubulins. Based on these results, we hypothesize that

mann, & Lehner, 2017). The a-tubulin showing upregulation in the

E. baikalensis

populations

contain

both

genetic

variation and

BOWMAN

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ET AL.

transcriptional phenotypic plasticity in response to higher temperatures, providing potential to survive in warmer environments and to respond to selection pressures imposed by such environments.

ACKNOWLEDGEMENTS We are grateful to the Lake Baikal Dimensions of Biodiversity consortium members, the crews of research vessels “Professor Treskov” and “Professor Kozhov” and to faculty and staff of Irkutsk State University Bolshie Koty field station for assistance with sample collection and to Marianne Moore, Tedy Ozersky and Peter Fields for useful suggestions on the analysis and manuscript preparation. Keur€ tterer and Dan cien Luu, Michael Blum, Robert Kofler, Christian Schlo Koboldt have been very helpful assisting us with their software products use. This work was supported by US National Science Foundation grant 1136710 to LYY and Russian Science Foundation grant 17-14-01063 to MAT. LLB was supported by US NSF Graduate K-12 Fellowship (DGE 0742364) and the Denise I Pav research award (ETSU). LYY designed the research, led the field collections, analysed the data and wrote the manuscript. LLB, ESK and MAT assisted in the research design, fieldwork and data analysis.

DATA AVAILABILITY The following sequence data files are available at NCBI: 454 cDNA reads, Accession number SRX3044558; Illumina cDNA reads from 38 samples (PRJNA395558; see Supporting information Table S1 for individual Accession numbers); assembled partial transcriptome, Accession numbers GFUA01000001:GFUA01005413. Bash shell, R and JMP scripts necessary to recapitulate downstream analyses and the following supplementary data files are available at Dryad (https://doi.org/ 10.5061/dryad.6058j04): SupplementaryData1_SNPs.xlsx (SNP data), SupplementaryData2_Transcripts.xlsx (Transcripts data), SupplementaryData2_Transcripts.jmp (Transcripts data, JMP format) and SupplementaryData3_TranscriptsDE.xlsx (Differential expression data).

AUTHOR CONTRIBUTION L.Y.Y. and M.A.T. designed the study, L.L.B., L.Y.Y. and E.S.K. participated in field work, L.L.B. and L.Y.Y. did the analysis, all authors contributed to writing and editing the manuscript.

ORCID Lev Y. Yampolsky

http://orcid.org/0000-0001-7680-6025

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SUPPORTING INFORMATION Additional supporting information may be found online in the Supporting Information section at the end of the article.

How to cite this article: Bowman LL, Kondrateva ES, Timofeyev MA, Yampolsky LY. Temperature gradient affects differentiation of gene expression and SNP allele frequencies in the dominant Lake Baikal zooplankton species. Mol Ecol. 2018;00:1–16. https://doi.org/10.1111/mec.14704

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