Bulletin of the Southern California Academy of Sciences
Volume 117 | Issue 2 Article 6
2018
Phylogenetic Study of Dioecious and
Parthenogenetic Populations of Canthocamptus
staphylinus (Crustacea, Copepoda, Harpacticoida)
Elena Kochanova
Institute of Biology of the Komi Scientific Center of the UB of the RAS, kochanova91@gmail.com
Jouko Sarvala
University of Turku, Finland, jouko.sarvala@utu.fi
Elena Fefilova
Institute of Biology of the Komi Scientific Center of the UB of the RAS, fefilova@ib.komisc.ru
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Recommended Citation
Kochanova, Elena; Sarvala, Jouko; and Fefilova, Elena (2018) "Phylogenetic Study of Dioecious and Parthenogenetic Populations of
Canthocamptus staphylinus (Crustacea, Copepoda, Harpacticoida)," Bulletin of the Southern California Academy of Sciences: Vol. 117:
Iss. 2.
Available at: https://scholar.oxy.edu/scas/vol117/iss2/6
Phylogenetic Study of Dioecious and Parthenogenetic Populations of
Canthocamptus staphylinus (Crustacea, Copepoda, Harpacticoida)
Cover Page Footnote
We thank Lauri Arvola, John Loehr and all staff of the Lammi Biological Station of Helsinki University for
help with sampling material from Lake Pääjärvi; Тarmo Тimm (Estonian University of Life Sciences, Centre
for Limnology, Tartu, Estonia) for help with sampling harpacticoids in Estonia; Natalia M. Sukhikh and Victor
R. Alekseev (Zoological Institute RAS, St. Petersburg, Russia) for providing samples, Matti Räsänen
(University of Turku) for help with the literature on the Baltic Sea history, Varpu Vahtera (University of
Turku) for useful comments and Charles Miller (Oregon State University) for the help with English editing.
Constructive comments by two referees helped to improve the focus of the paper. Our research was supported
by RFBR grants: 17-04-00337-a, 17-04-00027, Complex UB RAS Programs № АААА-А18-118011390005-9;
and performed in the frame of the state task of Department of Animals Ecology of the Institute of Biology of
the Komi Scientific Center of UB of RAS (№ АААА-А17-117112850235-2): Distribution, systematics and
spatial organisation of fauna and animals population in taiga and tundra landscapes and ecosystems at the
Northeast European.
This article is available in Bulletin of the Southern California Academy of Sciences: https://scholar.oxy.edu/scas/vol117/iss2/6
Bull. Southern California Acad. Sci.
117(2), 2018, pp. 138–149
© Southern California Academy of Sciences, 2018
Phylogenetic Study of Dioecious and Parthenogenetic Populations of
Canthocamptus staphylinus (Crustacea, Copepoda, Harpacticoida)
Elena Kochanova,1,2∗ Jouko Sarvala,3 and Elena Fefilova1
1Institute of Biology, Komi Scientific Center, Ural Branch of the Russian Academy of
Sciences, Syktyvkar, Russia, 167000
2Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia, 199034
3Department of Biology, University of Turku, Turku, Finland, FI-20014
Abstract.—The phylogenetic relationships of four dioecious populations and one
parthenogenetic population of the harpacticoid Canthocamptus staphylinus (Jurine,
1820) were studied. Analysis of the mtCOI gene revealed two main clades as a phy-
logenetic tree and a network of haplotypes: a clade with Fennoscandian populations
in Lake Pääjärvi (Finland) and Lake Vänern (Sweden), and a second clade with pop-
ulations in Lake Võrtsjärv (Estonia), Orlov Pond in Saint Petersburg (Russia), and
the type locality of the species in Lake Geneva (Switzerland). The parthenogenetic
population of C. staphylinus showed the smallest nucleotide and haplotype polymor-
phisms and could have evolved as a reaction to the changing environmental conditions
following the Last Glacial Maximum, 20K YBP.
The harpacticoid copepod Canthocamptus staphylinus (Jurine, 1820) is one of the most
widely distributed freshwater harpacticoid species in the Palearctic region (Lang 1948;
Borutzky 1952; Fefilova 2015). Normally, it is a stenothermal and psychrophilic form and,
according to different sources, inhabits waterbodies with temperatures ranging from 10° to
19°C (Sarvala 1979a). As part of the life cycle, adult C. staphylinus rests encysted in the bot-
tom mud. Discovery of the species in different types of water bodies — from small spring
pools to large lakes and rivers — indicates its high environmental plasticity. Individuals
are both geographically and ecologically variable in several morphological characteristics,
including the structure of the fifth pair of thoracal legs, numbers of spinules on the anal
operculum, form of the spermatophore, and the development of the aesthetask borne on
the fourth segment of the antennule (Lang 1948; Borutzky 1952; Fefilova 2015). This vari-
ability suggests that the forms described as C. staphylinus in the literature may actually
represent a group of closely related species.
Breeding of harpacticoid copepods is commonly dioecious. They possess clear sex-
ual dimorphism — females are usually larger than males and have different mor-
phologies of antennules and swimming legs (Borutzky 1952; Huys and Boxshall 1991;
Suárez-Morales 2015). However, parthenogenetic reproduction has been verified in a few
harpacticoid species. The first reports were for Elaphoidella bidens (Schmeil, 1894) and
Epactophanes richardi Mrazek, 1893, both from the family Canthocamptidae. For C.
staphylinus a parthenogenetic life cycle was proved to occur in the stock living in the olig-
otrophic Finnish Lake Pääjärvi. There are both field data (males comprised only 0.28% of
adults) and laboratory observations (unmated females isolated as nauplii or copepodids
and reared individually in the laboratory, produced viable offspring) (Sarvala 1979a). In
∗ Corresponding author: kochanova91@gmail.com
138
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PHYLOGENETIC STUDY OF HARPACTICOID COPEPOD 139
Table 1. Canthocamptus spp. sampling sites.
Country, Number of
No. area Locality Coordinates individuals Abbreviations
1 Geneva,
Switzerland
Lake Geneva 46°27′N, 06°31′E 8 Geneva
2 Hämeenlinna,
Finland
Lake Pääjärvi 61°04’N, 25°08’E 11 Paajarvi
3 Estonia Lake Võrtsjärv 57°40’N, 26°40’E 5 Vortsjarv
4 St. Petersburg,
Russia
Orlov Pond 59°51′N, 30°02′E 10 SPB
5 Sweden Lake Vänern 58°55′N, 13°30′E 9 Vanern
6 Syktyvkar, Komi
Republic,
Russia
A pond in the
Botanical
Garden
61°40′N, 50°49′E 1 C. microstaphyli-
nus
addition, parthenogenesis has been suspected on the basis of the scarcity of males in some
other Elaphoidella species: E. leruthi Chappuis, 1937 and E. elaphoides (Chappuis, 1924)
in the northernmost part of their range (Chappuis 1955), and E. grandidieri (Guerne and
Richard, 1893).
For different types of invertebrate animals, a parthenogenetic life style serves as an adap-
tation to unfavorable environmental conditions (Clark and Bowen 1976; Glesener and
Tilman 1978; Grebelnyi 1996; Hebert and Finston 2001; Hebert et al. 2007; Weeks et al.
2008). Asexual or parthenogenetic organisms occur more often at higher latitudes and al-
titudes, on islands and in environments variously classified as marginal, stressful, transient
or disturbed (Cuelar 1977; Glesner and Tilman 1978; Bell 1982; Lynch 1984; Suomalainen
et al. 1987). Although clonal reproduction is expected to be reproductively advantageous
(Maynard-Smith 1978; Bell 1982), obligately asexual organisms are short-lived on geologic
time scales and have been regarded as evolutionary dead ends (Bell 1982; Lorenzo-Carballa
et al. 2012.). However, in the short term, switching to an asexual mode can help organisms
to exploit a narrow spectrum of environmental resources more efficiently than could genet-
ically diverse sexual populations (the “demographic balance” hypothesis, Gets 2001; Haag
and Ebert 2004). Molecular responses to environmental changes are modulated by pheno-
typic plasticity (physiological acclimatization) and genetic adaptation (genetic evolution
through natural selection under new environmental conditions) and may play important
roles in the persistence of the species (Smolina 2015). To reveal the phylogenetic relation-
ships among parthenogenetic and dioecious populations of C. staphylinus we studied the
genetic population structure of this species across a wide geographic area using mitochon-
drial DNA sequence data.
Material and Methods
Samples were collected from 2015 to 2016 from four dioecious populations of
C. staphylinus (including the type locality of the species in Lake Geneva, Switzerland)
and one parthenogenetic population in Lake Pääjärvi. In addition, a population of
Canthocamptus microstaphylinus Wolf, 1905 was sampled in 2015 in Syktyvkar, Komi Re-
public, Russia and used as a group for comparison with closely related species. Samples
from the Orlov pond and Lake Geneva were collected by Natalia M. Sukhikh in November
2010 (Table 1, Fig. 1). All samples were collected close to the shore with a hydrobiological
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Fig. 1. Sample locations of specimens of Canthocamptus spp. examined in this study. Locality names
are listed in Table 1.
100-μm mesh hand net. Organisms in these samples were preserved in 96% alcohol solu-
tion. Morphological identification of species was performed using an ES Bimam R 13-1
Microscope (Russia), and Micromed MC-4-Zoom Led stereoscopic microscope (Russia)
according to the descriptions by Lang (1948).
A 611 base pair (bp) fragment of the mitochondrial cytochrome oxidase I (mtCOI)
gene was sequenced from 44 adult copepods. Genomic DNA was extracted from cope-
pods preserved in 96% ethanol following protocols outlined in Walsh et al. (1991). Specif-
ically, the bodies of each crustacean were added to 5% Chelex-100 (Sigma-Aldrich,
St Louis, MO, USA) solution in bidistilled water. Samples were spun for 30 s at
12,000 rpm. The mixture was incubated at 90°C for 30 min, then spun for 30 s
at 12,000 rpm. Samples were incubated at 90°C for 15 min and spun for 15 s at
12,000 rpm. Then samples were stored at −20°C and amplified through PCR. Univer-
sal primers LCO1490 (5′-GGTCAACAAATCATAAAGATATTGG-3′) and HCO2198
(5′TAAACTTCAGGGTGACCAAAAAATCA-3′) (Folmer et al. 1994) were used for am-
plification of COI by polymerase chain reaction (PCR). PCR started with DNA denaturing
at 95°C (60 s), followed by 35 cycles of 30 s denaturing at 95°C, 30 s annealing at 50°C, and
50 s extension at 72°C, and then a final extension at 72°C for 7 min (Lee 1999). The prod-
uct was purified with a Qiaquick PCR purification kit and sequenced in an ABI Prism 310
automated sequencer. To avoid mistakes in sequences we used bi-directional sequencing
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PHYLOGENETIC STUDY OF HARPACTICOID COPEPOD 141
Table 2. Percent genetic distances for the six populations of Canthocamptus spp. based on mtCOI
sequences.
Population Pääjärvi Vänern SPB Võrtsjärv Geneva
Pääjärvi
Vänern 2.5
SPB 22.5 22.1
Võrtsjärv 23.5 23.7 3.1
Geneva 23.4 23.1 2.1 1.2
C. microstaphylinus 25.5 27.0 26.8 26.2 26.6
with above mentioned primers. In case of double peaks or ambiguous base calls each se-
quence was compared with obtained chromatograms, a signal that exceeded the other was
taken into account. All processing was done at the Center for Collective Use “Molecular
Biology” of the Institute of Biology, part of the Komi Scientific Center of the Ural Branch
of the Russian Academy of Science.
Nucleotide sequences were aligned with the algorithm CrustalW and corrected manu-
ally (due to several shifts of nucleotide motifs after alignment) using the program pack-
age Geneious (version 7.0.6.) (Kearse 2012). Phylogenetic trees were also constructed in
Geneious using a Maximum Likelihood method with a high level of the bootstrap coeffi-
cient (1000 replications). A median network of haplotypes was constructed with Network
4.6.1.3 (Bandelt 1999). Statistical analysis of the DNA polymorphism was performed in
DNAsp 5.10 (Librado 2009). All sequences of C. staphylinus were registered in GenBank
under the accession numbers KP974713–KP974719 and MG209708-MG209737. In ad-
dition, a sequence of C. microstaphylinus (accession number KP974734.1) sampled and
sequenced according to methods described above was included in the phylogenetic anal-
ysis. For comparison, three further sequences obtained from GenBank were added: C.
staphylinus from Northern Germany (MF077881.1), Canthocamptus coreensis Chang, 2002
(KT030277.1) and Elaphoidella humphreysi Karanovic, 2006 (JN039173).
Results
A total of 43 C. staphylinus females were sequenced for the mtCOI gene. Males were
observed in all populations except the parthenogenetic one in Pääjärvi. Moreover, some of
the females in Pääjärvi were bearing egg sacs but had no spermatophores attached to their
bodies, suggesting that mating had not taken place for these individuals.
Phylogenetic analysis revealed two strongly separated clades with maximum pairwise
divergences of 23.7% between geographically separate populations (Fig. 2, Table 2). All
clades were strongly supported by bootstrap percentages and were divided mostly accord-
ing to the populations’ geographical locations. The clade I was common for three pop-
ulations of the species C. staphylinus: the type locality in Lake Geneva, Orlov Pond in
Saint Petersburg and Lake Võrtsjärv. These three populations formed three main groups
that roughly but not completely followed their geographical origin with genetic diver-
gences between them varying from 1.2% to 3.1%. Two sequences of C. staphylinus from
Orlov pond were placed in the group for Lake Geneva sequences, while two sequences of
the species from Lake Geneva fell into groups for Lake Võrtsjärv and Orlov pond. The
clade II included two subclades, consisting of the parthenogenetic population from Lake
Pääjärvi and the dioecious population from Lake Vänern together with the sequence of
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Fig. 2. Phylogenetic tree of the relationship between Canthocamptus staphylinus populations based
on data from mitochondrial cytochrome oxidase subunit I (COI) region (611 bp) by the maximum
likelihood method. Numbers beside nodes indicate bootstrap values. As an outgroup, a sequence of
Elaphoidella humphreysi from NCBI was used (accession number JN039173). From GenBank, a sequence of
C. staphylinus from northern Germany (accession number MF077881), a sequence of Canthocamptus mi-
crostaphylinus (accession number KP974734.1), and a sequence of Canthocamptus coreensis (accession num-
ber KT030277.1) were also included.
C. staphylinus sampled in Northern Germany with genetic divergence of 2.5% between
them.
The COI haplotype network formed two separate clades similar to those dis-
tinct in the phylogenetic tree (Fig. 3). The total number of haplotypes was 22. The
C. staphylinus clade II consisted of the parthenogenetic population from Pääjärvi and
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PHYLOGENETIC STUDY OF HARPACTICOID COPEPOD 143
Fig. 3. Haplotype network based on statistical parsimony, representing genealogical relationships be-
tween mtCOI haplotypes in sexual and parthenogenetic populations of Canthocamptus staphylinus. Num-
bers in square brackets and hash marks represent mutations between haplotypes. The size of the circles
correlates with haplotype frequency. The dashed circles in the network indicate the three main clades with
a significant geographic association (see the main text).
the dioecious population from Vänern. The most frequent haplotype 1 in the haplotype
network belonged to the parthenogenetic population. The clade I was formed of the C.
staphylinus populations from Lake Geneva (the species type locality), Orlov Pond in Saint
Petersburg and Lake Võrtsjärv. The latter clade held a central position in the haplotype
network, with all other haplotypes extending away from it. Numbers of mutations were
100 between the first and the second clades.
Analyses of the sequence polymorphism of the populations allocated to C. staphylinus
are summarized in Table 3. Among 43 obtained sequences, there were 22 haplotypes, and
135 polymorphic sites with 147 mutations. General haplotype and nucleotide diversities
were 0.920 and 0.1067, respectively. The haplotype and nucleotide diversities observed in
the parthenogenetic population were lower than in the dioecious populations. The small-
est numbers of polymorphic sites and mutations were detected in populations from Lake
Pääjärvi and Lake Võrtsjärv.
Table 3. Polymorphism of the COI gene from Canthocamptus staphylinus populations. n — number
of sequences, N — Number of haplotypes, Hd — Haplotype diversity, L — length of sequences, Pi —
Nucleotide diversity, S — Number of polymorphic (segregating) sites, Eta — number of mutations. The
parthenogenetic population is indicated in bold.
Population n N Hd L Pi S Eta
Pääjärvi 11 2 0.182 611 0.00033 1 1
Vänern 9 9 1.000 611 0.00884 18 18
SPB 10 5 0.756 611 0.01118 20 20
Võrtsjärv 5 2 0.400 611 0.00066 1 1
Geneva 8 4 0.643 611 0.00702 17 17
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Discussion
The demographic advantage of obligate parthenogenesis for aquatic invertebrates is
the possibility of accelerating the life cycle during a short period of favorable conditions
(Lynch and Gabriel 1983; Hebert and Hann 1986). In copepods, parthenogenetic repro-
duction has remained poorly known, reflecting that it is a rarity in nature and uncommon
for this taxon. As was mentioned above, in a few species of harpacticoids of the family Can-
thocamptidae parthenogenesis has been suspected because males are rarely found, and in
some of those species laboratory experiments show that females can reproduce by them-
selves without males (Sarvala 1979a; Dole-Oliver et al. 2000; Guterrez-Aguirre et al. 2011).
Across the distributional range of C. staphylinus, only one parthenogenetic population is
known, that from Lake Pääjärvi (and possibly another population at 80 km distance from
it). All other populations studied, including those of the present work, were dioecious with
males present in every population (Smyly 1957; Sarvala 1979a; Dole-Oliver et al. 2000;
Fefilova 2015). The parthenogenetic population of E. richardi was also described from the
Scandinavian region. Moreover, E. richardi var. angulatus Kulhavi, 1957 hatched out from
parthenogenetic eggs, was able to develop and reproduce sexually with sperm transfer from
males to females (Lang 1935; Borutzky 1952).
Many species of copepods have female-biased adult sex ratios (Kiørboe 2006). A variety
of factors have been suggested to influence the sex determination in this taxon: temperature
(Katona 1970); food (Irigoien et al. 2000); population density (Heinle 1969) and pressure
(Vacquier and Belser 1965). For example, in Calanus spp. food quantity and quality have
a significant effect on the seasonally changing population sex ratio, supporting the exis-
tence of a strong environmental influence on sex determination (Svensen and Tande 1999;
Irigoien et al. 2000; Miller et al. 2005; Gusmão 2009).
Our analysis of genetic population structure reveals a broad range of genetic divergence
(1.2–23.7%) among populations of C. staphylinus (Fig. 2, Table 2). The genetic divergence
between clades of haplotypes also was large and generated a haplotype network with its
branches containing many mutations between populations (Fig. 3). Interestingly, the ge-
netic divergence between the two clades of C. staphylinus was similar to that between
C. staphylinus and closely related but separate species of C. microstaphylinus (more than
20%). This suggests the existence of a complex of at least two cryptic species among the
C. staphylinus populations. This complex would include a “northern” species with popu-
lations from Finland, Sweden and Northern Germany, and a “continental” species with
populations from Russia, Estonia and Switzerland (Fig. 2).
Similar unexpectedly wide genetic variability revealing the existence of several cryp-
tic forms has been found in other studies of molecular-genetic population structure of
harpacticoids. For example, in a study of Nannopus palustris Brady, 1880 genetic distances
of mtDNA reached up to 78% between populations and allowed to separate several cryp-
tic forms (Garlitzka et al. 2012). According to studies on phylogenetic and phylogeo-
graphic structure among populations of Tigriopus californicus (Baker, 1912) divergences
of mtDNA often exceeded 20% (Burton et al. 2007; Willet and Ladner 2009). High levels
of intra- and interspecific divergence seem to be widespread phenomena among members
of the order Harpacticoida (Schizas et al. 1999; Easton et al. 2010). In freshwater cope-
pod species, the observed molecular genetic divergence can be the result of founder effects
accompanied by limited gene flow between populations, even those in adjacent habitats
(Bucklin 1998).
The pattern of population structure which is observed in C. staphylinus is defined by the
present-day gene flow as well as the historical processes. The clade which consists of the
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PHYLOGENETIC STUDY OF HARPACTICOID COPEPOD 145
Pääjärvi and Vänern populations (Fig. 2) suggests that they have a common history. In-
deed, during the development of the Baltic Sea after the last Ice Age, the basins of Pääjärvi
and Vänern were both parts of the Yoldia Sea stage (10300–9500 years BP; Björck 1995),
the water of which was fresh for most of the time. While Lake Pääjärvi was already isolated
from the Yoldia Sea (Okko 1969), Lake Vänern became separated slightly later, at about
9500 years BP, just at the transition to the following Baltic freshwater stage, the Ancylus
Lake. Hence, the animal populations of these lakes would have close relationships.
The unexpected clear distinction between the Swedish and Finnish populations on one
hand, and the geographically rather close Võrtsjärv and Saint Petersburg populations on
the other hand, indicating long isolation of these populations, also becomes understand-
able on the basis of existing data on the geological history of the area. The continental ice
started to retreat from Estonia around 13000 years BP and had disappeared by 11000 years
BP (Moora et al. 2002). There was an Ice Võrtsjärv up to 12200 years BP, partly dammed
by ice, followed by Big or Ancient Võrtsjärv during 12200–7500 or 7000 years BP, after
which there has been the contemporary lake. Võrtsjärv was thus from the beginning sepa-
rated from the successive stages of the Baltic basin. The same applies to most of the Saint
Petersburg region. The distance between Võrtsjärv and Saint Petersburg is not so great,
around 700 km, and resting stages in the form of cysts might allow more efficient dispersal
than is the rule in harpacticoids.
The similarity of the populations from Võrtsjärv and Saint Petersburg with that from
Lake Geneva (Figs. 2 and 3) is more difficult to explain on the basis of existing geological
information. The overlapping structure of the distribution of sequences in the phylogenetic
tree and the haplotype network together with relatively small genetic differences in spite of
considerable geographical distances suggests that these populations might have an ancient
history of dispersal long before than the last Ice Age. The relationships between these
harpacticoid populations represent a similar problem as the present-day distributions of
the so-called “glacial relicts” in and around the Baltic Sea, which have been much discussed
relative to the improving knowledge of the geological history (Segerstråle 1982). Even in
case of the “glacial relicts” the explanations have remained speculative.
A detailed analysis of the distribution patterns of dioecious and parthenogenetic forms
of insects was carried out by Suomalainen and collaborators (Suomalainen and Saura
1973; Suomalainen et al. 1976, 1987). It proved that the invasion of polyploid popula-
tions (which are common for asexual organisms like hermaphrodites and parthenogens)
occurred as a result of the Quaternary Glaciations. These polyploid insect populations
are supposed to have originated from diploid populations that survived to the end of the
glaciation in the Central European mountains. Moreover, some diploid populations are
still capable of parthenogenetic reproduction (Grebelnyi 1996).
Analysis of mtCOI gene reveals that the parthenogenetic population of C. staphylinus
is a separate subclade on the phylogenetic tree and includes two separate haplotypes with
only one mutation between the distinct sequences (Figs. 2 and 3). In addition, the smallest
values of haplotype and nucleotide diversity were observed for this population (Table 3).
These facts support the suggestion that the parthenogenetic population of C. staphylinus
has a clonal genetic structure. Usually, in sexual reproduction, mitochondrial genes are
inherited exclusively from the mother (Travis 2000). The mtCOI gene shows rapid evo-
lutionary rates, lack of introns and genetic recombination and allows to trace maternal
lineage far back in time (Meyer 1993). In view of this, the clonal genetic structure from the
observed parthenogenetic population points out that the males’ genetic information was
restricted during several generations.
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The small genetic distance between the Vänern and Pääjärvi populations suggests that
parthenogenesis in C. staphylinus in Pääjärvi might be of relatively recent origin. This idea
was mentioned previously with statements of restricted distribution and high embryonic
mortality in the parthenogenetic population (Sarvala 1979a). In some species of millipedes,
parthenogenetic and dioecious populations were also mixed in one clade of the phyloge-
netic tree (Short and Vahtera 2017), suggesting that parthenogenesis may have evolved
more recently as a specific adaptation to certain environmental conditions without chang-
ing the structure of nucleotide sequences.
As a rather big and fast-growing harpacticoid, C. staphylinus has relatively high food
requirements, and thus prefers eutrophic environments (Sarvala 1979a,b; Hämäläinen and
Karjalainen 1996). However, Lake Pääjärvi is oligotrophic, and food seems to be a limit-
ing factor for the species. Under such conditions, the parthenogenetic mode of reproduc-
tion should give a selective advantage. Females of C. staphylinus from the parthenogenetic
population of Lake Pääjärvi can copulate if males are present, but only few males are
produced (Sarvala 1979a). Likewise, even other populations of C. staphylinus are often
strongly female-biased (Lilljeborg 1902; Bevercombe 1973; Young 1974), or the numbers
of males decrease during cold periods (Donner 1928; Smyly 1957).
Clearly, further studies of other populations of C. staphylinus (dioecious and possi-
bly parthenogenetic), and possibly other species of this genus are needed to clarify both
the taxonomy of this complex of species and the phenomenon of parthenogenesis in
Canthocamptidae.
Conclusions
1) The harpacticoid species C. staphylinus shows a high level of genetic divergence
between populations.
2) The parthenogenetic population of C. staphylinus from Lake Pääjärvi was geneti-
cally similar to the dioecious population from Lake Vänern, suggesting a relatively
recent origin of parthenogenesis in this taxon.
3) The parthenogenetic population showed the smallest nucleotide and haplotype
diversity, suggesting a clonal genetic structure in the population through the line
of maternal inheritance of mitochondrial DNA.
4) The “northern” and “continental” clades of C. staphylinus can likely be considered
as a complex of cryptic species.
Acknowledgments
We thank Lauri Arvola, John Loehr and all staff of the Lammi Biological Station of
Helsinki University for help with sampling material from Lake Pääjärvi; Тarmo Тimm
(Estonian University of Life Sciences, Centre for Limnology, Tartu, Estonia) for help with
sampling harpacticoids in Estonia; Natalia M. Sukhikh and Victor R. Alekseev (Zoologi-
cal Institute RAS, St. Petersburg, Russia) for providing samples; Matti Räsänen (Univer-
sity of Turku) for help with the literature on the Baltic Sea history; Varpu Vahtera (Uni-
versity of Turku) for useful comments; and Charles Miller (Oregon State University) for
the help with English editing. Constructive comments by two referees helped to improve
the focus of the paper. Our research was supported by RFBR grants: 17-04-00337-a, 17-
04-00027, Complex UB RAS Programs No. АААА-А18-118011390005-9; and performed
in the frame of the state task of Department of Animals Ecology of the Institute of Bi-
ology of the Komi Scientific Center of UB of RAS (No. АААА-А17-117112850235-2):
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Distribution, systematics and spatial organization of fauna and animal populations in
taiga and tundra landscapes and ecosystems at the Northeast European.
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