3Natural History Museum of Latvia,. LV 1050 Riga, Latvia. Dalius Butkauskas1,*, Saulius Å važas1, Vaida TubelytÄ2, Julius MorkÅ«nas1, Aniolas Sruoga1,2,.
Cent. Eur. J. Biol. • 7(5) • 2012 • 886-894 DOI: 10.2478/s11535-012-0065-9
Central European Journal of Biology
Coexistence and population genetic structure of the whooper swan Cygnus cygnus and mute swan Cygnus olor in Lithuania and Latvia Research Article
Dalius Butkauskas1,*, Saulius Švažas1, Vaida Tubelytė2, Julius Morkūnas1, Aniolas Sruoga1,2, Dmitrijs Boiko3, Algimantas Paulauskas2, Vitas Stanevičius1, Vykintas Baublys2 Institute of Ecology, Nature Research Centre, LT 08412 Vilnius, Lithuania
1
Department of Biology, Vytautas Magnus University, LT 44404 Kaunas, Lithuania
2
Natural History Museum of Latvia, LV 1050 Riga, Latvia
3
Received 29 February 2012; Accepted 15 May 2012
Abstract: Two closely related swan species, the mute swan Cygnus olor and the whooper swan Cygnus cygnus, were formerly allopatric throughout their breeding ranges, but during the last decades a sympatric distribution has become characteristic of these species in the Baltic Sea region. The whooper swan has gradually replaced the mute swan in many suitable habitats in Lithuania and Latvia. Marked differences in the genetic population structure of both species may partially explain the dominance of the whooper swan, as genetic population divergence can be a major factor affecting inter-specific competition. A homogenous genetic population structure was defined for mute swans breeding in Lithuania, Latvia, Poland and Belarus. Breeding mute swans in this region are mostly of naturalised origin. A diverse population genetic structure characterizes whooper swans breeding in Lithuania and Latvia. Keywords: Cygnus cygnus • Cygnus olor • D-loop • population genetic structure • Coexistence © Versita Sp. z o.o.
1. Introduction Coexistence between closely related species in a given habitat or region has been of interest to researchers for decades [1-4]. Species with diverse population structures are generally better adapted to changing environmental conditions and can more successfully utilize new types of habitats [5]. As a result of global environmental change, closely related species that were historically separated by geographic barriers are sometimes found to coexist, which can result in an increase in interactions such as competition and hybridization. Two closely related swan species, the mute swan Cygnus olor and the whooper swan Cygnus cygnus were formerly allopatric throughout their breeding ranges, but during the last decades their breeding ranges have overlapped in the Baltic Sea Region [6-8]. This range overlap was caused by a rapid expansion in the breeding range of both species in Europe. In
886
Lithuania and Latvia both species presently occur in the same type of habitats. The whooper swan is a characteristic species of the boreal zone in Europe. It was pushed close to extinction in the Baltic region during the 19th and the early 20th century due to intense human persecution [6]. A rapid range expansion of the species has been recorded since the 1970s (mainly due to improved conservation measures) and during the past decades it has established as a breeding species in all countries of the Baltic region. In Sweden, the number of whooper swans has increased from 20 pairs in the early 20th century to about 5.400 pairs estimated during the last few years [9]. Similarly in Finland, a recorded 15 pairs from the 1940s have increased to 5.000–7.000 pairs during the last decade [10]. An increase in the number of the breeding birds was also recorded in other countries of Central and Western Europe [11-16]. The species continues to spread southwards, re-occupying former nesting grounds. During the same period, since the * E-mail: dalius@ekoi.lt
D. Butkauskas et al.
1970s, a marked northwards breeding range expansion of the species was recorded in tundra zone of Northern Europe [17,18]. The mute swan, a species characteristic of the temperate zone of Europe, has recently re-established itself as a breeding species in the whole Baltic Region, NW Russia and Belarus [6,11,16,19-21]. The local wild stocks in the Baltic States were hunted to extinction in the 18th–19th centuries [22]. The newly established breeding populations were probably formed by individuals of naturalised origin. This species has long been domesticated for human consumption in Europe [23]. Naturalised stocks of this species are dominant in Western Europe [6]. During the last several decades, the breeding range of mute swans has expanded up to 2000 kilometers northwards [17,24,25]. The aim of this study was to analyze how the coexistence of two closely related swan species affect their distribution in different habitats in Lithuania and Latvia and to identify the population genetic structure characteristic of both species, as genetic population divergence can be a major factor impacting interspecific competition between both species.
2. Experimental Procedures 2.1 Data collection on swan populations
All available information concerning the long-term changes in number, distribution and habitat use of breeding populations of mute and whooper swans in Lithuania and Latvia was analyzed. The abundance and distribution of breeding populations of swans in Lithuania and Latvia have been reviewed earlier [7,11,22,26-34]. Detailed, country-wide surveys of mute and whooper swans were conducted in Latvia between 2003–2009 ad in Lithuania between 2008–2011. Studies of the whooper swan in all known nesting sites in Lithuania were implemented. The habitat preference of mute and whooper swans was determined. The abundance and habitat selection of whooper Swans in Latvia were investigated [16].
2.2 Sampling of birds for DNA analysis
Permission for collection of material was given by the Ministry of Environment of Republic of Lithuania (Nr.(11-1)-D8-2614) on 28 of March 2008. Blood samples were collected from 51 whooper swans and 45 mute swans in 2009-2011. Whooper swan blood samples of were collected from 17 breeding adult birds or juveniles from Lithuania, and 15 from Latvia. In addition, six moulting whooper swans were sampled in Lithuania in July - August. One whooper swan sampled in Lithuania
was of Polish origin and 8 migratory birds sampled in their stop-over sites in Lithuanian coastal wetlands in March were of unknown origin. Feathers collected from four whooper swans breeding in Iceland and wintering in the United Kingdom were also analysed. Mute swan blood samples were collected from 21 individuals from the Lithuanian breeding population sampled in their moulting sites and from 24 birds wintering in Lithuania. It is likely that most of these wintering birds were local breeders. According to the ringing recoveries among the sampled wintering birds, two birds originated from Belarus, four from Latvia and one from Poland. Blood was taken from the medial metatarsal vein of the captured birds and collected directly into EDTA-coated vials after pricking the blood vessel with a sterile sharp needle [35,36]. Samples were refrigerated at -20°C until DNA extraction. Feathers suitable for DNA extraction were collected and placed in paper envelopes and stored at room temperature [37].
2.3 Extraction of DNA, PCR procedures and sequencing DNA was extracted from blood and feather samples using universal and rapid salt-extraction of genomic DNA for PCR-based analysis [38]. Extracted DNA was dissolved in water and stored at -20°C. Initially, a Cygnus sp. species-specific primer pair (forward primer Cygn-1F: 5’-GGTTATGCATATTCGTGCATAGAT-3’, reverse primer Cygn-1R: 5’- TTCCACAGATGCCACTTTGA-3’) was constructed using the software Primer 3 (http://frodo.wi.mit.edu/primer3) [39]. The designation of primers was based on conservative fragments detected after the homological sequence alignment of the available Gene Bank D-loop sequences of swans and related species’ of Anatidae (Cygnus atratus (Acc. No. FJ379295 in [40]), Branta leucopsis (AY112975 in [41]), Anser albifrons (AY112967 in [41]), Dendrocygna javanica (FJ379296 in [40]). PCR analysis was carried out in a total volume of 25 μl containing 125 ng of genomic DNA, 200 μM (each) dNTPs, 0.1 μM forward primer, 0.1 μM reverse primer, 2.5 μM MgCl2, 1 U Taq DNA Polymerase (MBI Fermentas, Lithuania). The PCR was performed using Mastercycler® Gradient (Eppendorf) using the following temperature profile: 35 cycles at 94°C for 45 s, 54°C for 45 s, and 72°C for 1 min, proceeded by 2 min at 95°C and followed by a final elongation step for 5 min at 72°C. The quality and size of the amplified DNA fragments was verified in 1.5% agarose gel and purified by Shrimp Alkaline Phosphatase (SAP, Fermentas, 1 u/μl) and FastAP™ thermosensitive alkaline phosphatase (ExoI, Fermentas, 10 u/μl) nucleases for 15 min at 37°C and then for 15 min at 85°C. The amplified fragments were 887
Coexistence and population genetic structure of the whooper swan Cygnus cygnus and mute swan Cygnus olor in Lithuania and Latvia
sequenced by the ABI 3130xl automatic sequencer using the primers Cygn-1F and Cygn-1R and BigDye® Terminator v3.1 Cycle Sequencing Kit.
2.4 Statistical analysis
Sequencing results were analysed using CLC Free Workbench (CLC bio A/S, version 3.0, available at http://www.clcbio.com/index.php?id=27) and the identification of different haplotypes was carried out manually after the alignment of all determined sequences of the whooper and mute swans with the reference sequence of individual coded 7C96 (Acc. No. JQ693392). The nucleotide diversity (π), haplotype diversity (H), the number of polymorphic positions (S) and the number of mutations (η) were calculated using DNASP (version 5.10.01; available at http://www.ub.edu/dnasp). Relationships between haplotypes were estimated using molecular-variance parsimony techniques. The haplotype network was computed under haplotype pairwise differences, giving the number of mutation steps between haplotypes. The network was constructed by using Phylogenetic Network Analysis Software (Network version 4.600, available at www.fluxus-engineering.com). The phylogenetic tree was generated by the neighbour-joining method [42] using CLC Free Workbench version 4.0.1. Bootstrapping (100 replicates) was used to assess support for particular nodes in the resulting tree.
3. Results 3.1 Population development of the mute and whooper swan and their inter-specific competition
At the beginning of the 20th century, Lithuania was at the northern limit of the breeding range of the Palearctic population of the mute swan. Solitary breeding pairs were irregularly recorded in southern Lithuania in the early 20th century [22]. A marked increase in the Lithuanian breeding population has been recorded since the mid-20th century. The total number of breeding mute swans in Lithuania has increased from 26 pairs in 1955 up to 1.000 pairs in the 1990s [30,31]. In 2010–2011 the local population of mute swans was estimated to be at up to 1.500 pairs of breeding birds and about 3.000 non-breeding individuals. A rapid increase in number was also recorded in Latvia, where the local population increased from several pairs in the early 20th century to up to 450 pairs in the 1980s [11]. The breeding population of the whooper swan has increased in Lithuania from a single pair recorded in 1987 to 80 pairs registered in 2011. In 2010–2011, breeding whooper swans were found in most regions of Lithuania. 888
In Latvia, the breeding population has increased from a single nest found in 1973 to up to 260 pairs estimated in the last few years [16]. The main breeding area of the whooper swan was found in the western part of Latvia. Large, shallow, eutrophic lakes were the principle breeding centers of mute swans in Lithuania and Latvia in the 1950s–1960s [22,43]. Between 1970 and 1990 a large part of the Lithuanian population of the mute swan switched from natural to man-made wetlands (fishponds, water reservoirs, park ponds, exploited gravel pits, etc.) [31]. During the last few decades, large fishpond complexes supported about 40% of all mute swans breeding in Lithuania [33]. Fishponds are also the principal breeding habitats of the whooper swan in Lithuania and Latvia. During the past few years, fishponds supported about 60% of all whooper swans breeding in Lithuania and about 80% of those found in Latvia [7,16]. The results of this study indicate that mute swans are gradually withdrawing from their preferred nesting habitats in Lithuania, potentially due to the aggressive territorial behaviour of the whooper swan. In 2009–2011, whooper swans replaced mute swans in at least seven nesting sites located in different parts of Lithuania. In most cases, encounters between whooper swans and mute swans were observed in fishponds and in all cases, pairs of mute swans were ousted from their nesting sites by aggressive males or pairs of whooper swans. During the past decades in Latvia, whooper swans have gradually replaced mute swans in most artificial ponds located in the western part of the country [7,16].
3.2 Population genetic structure of the mute and whooper swan Partial mitochondrial D-loop sequences of approximately 417 bp in length were determined for 51 analysed whooper swans and 45 mute swans. Alignment of all 45 sequences of mute swan revealed only one haplotype (Acc. No. JQ693393) suggesting that monotypic genetic structure is characteristic of mute swans breeding and wintering in Lithuania. Seventeen different mtDNA haplotypes were identified for whooper swans with 18 polymorphic nucleotide sites (excluding insertions/deletions), which accounted for 4.32% of a sequenced 417 bp fragment (Table 1). Among these polymorphic sites, there were 16 transitions and three transversions. The mtDNA sequence comparison of the complete whooper swan alignment revealed 7 C↔T and 9 A↔G transitions, 1 C↔A, 1 T↔G and 1 G↔C transversions. On the basis of the unrooted statistical parsimony network derived from D-loop sequences of whooper swans, two different haplogroups “A” and “B” were identified. Twelve different haplotypes were treated as belonging to haplogroup “A”
D. Butkauskas et al.
Number of indv. per sampling place**
Variable sequence positions* 5
23
34
70
71
90
94
98
99
119
123
135
202
211
226
235
271
380
Haplo-type
LT
A01
A
C
A
A
A
C
T
C
G
C
T
A
C
A
T
G
G
A
3
A02
•
•
•
•
•
•
C
•
•
•
•
•
•
•
•
•
•
•
4
4
A03
•
T
•
•
•
•
C
•
•
•
•
•
•
•
•
•
•
•
1
1
A04
•
•
•
•
•
•
•
•
•
T
•
•
•
•
•
•
•
•
1
1
A05
•
•
•
•
•
•
•
T
•
•
•
•
•
•
•
•
•
•
3
3
A06
•
•
•
•
•
•
•
T
•
•
•
•
•
G
•
•
•
•
3
3
A07
•
•
•
G
•
•
•
A
•
•
•
•
•
•
•
•
•
•
1
1
A08
•
•
•
•
•
•
•
•
•
•
•
•
•
•
G
•
•
•
1
1
A09
G
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
3
3
A10
G
•
•
•
•
•
•
•
•
•
•
•
•
•
•
A
C
G
A11
•
•
•
•
•
•
•
•
•
•
•
•
T
•
•
•
•
•
1
1
A12
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
A
•
•
1
1
B01
•
•
•
•
•
T
C
•
A
•
C
•
•
•
•
•
•
•
6
B02
•
•
•
•
•
T
•
•
A
•
C
•
•
•
•
•
•
•
1
1
B03
•
•
G
•
•
T
•
•
A
•
C
•
•
•
•
•
•
•
1
1
B04
•
•
•
•
•
T
C
•
A
•
C
G
•
•
•
•
•
•
3
3
B05
•
T
•
•
G
T
C
•
A
•
C
•
•
•
•
•
•
•
3
3
Table 1.
LV
UK
Total
3
2
8
1
8
1
14
Whooper swan haplotypes identified by comparison of 417 bp D-loop partial sequences of birds sampled in Lithuania, Latvia and the United Kingdom in 2009-2011 (nucleotide positions numbered according to the reference D-loop sequence of Cygnus cygnus Acc. No. JQ693392).
*Polymorphisms inside the gap are omitted from this table. Dots indicate identity with haplotype A01 (GeneBank accession number JQ693392), letters equal base substitutions. **Bird sampling locations: LT – Lithuania, LV- Latvia, UK – United Kingdom.
and haplogroup “B” included another five haplotypes (Figure 1). At least three mutational steps separate closely related haplotypes belonging to the different haplogroups “A” and “B”. One common haplotype (A01) was found in whooper swans of Eastern Baltic origin (one bird breeding in Lithuania and three in Latvia) and in birds breeding in Iceland (two birds). One common haplotype (B01) was found in whooper swans breeding in Lithuania (four birds), Latvia (eight birds) and one Polish-origin bird sampled in Lithuania. One haplotype (A09) was common for breeders from Lithuania (one bird) and Latvia (two birds). Eight haplotypes (A02, A05, A07, A08, B02–05) were specific to breeders from Lithuania (13 birds), two haplotypes (A06, A10) were specific to breeders from Latvia (two birds) and two haplotypes (A11, A12) were specific to breeders from Iceland. Eight haplotypes (A01–04, A06, B01, B04–05) were detected in migrants of unknown origin sampled in Lithuania (12 birds).
Differences in haplotype number and frequency resulted in high haplotype diversity in whooper swans sampled in Lithuania, Latvia and the United Kingdom, with an average value of 0.879 (Table 2). Haplotype diversity differed slightly among the sampling areas with the lowest diversity found in birds breeding in Latvia (0.695) and the highest diversity in breeders from Lithuania (0.917). The current population genetic structure of whooper swans as revealed by haplotypic network reconstructions indicated previous historic isolation of different populations. The only defined mute swan haplotype differed from the most closely related sequence (haplotype A07) of the whooper swan by 8 mutational steps (Figure 1). The monotypic genetic structure of mute swans represented by a single haplotype has revealed a population genetic structure rarely recorded in wild species (Figure 2). The intraspecific genetic diversity of D-loop sequences with numerous haplotypes defined in 889
Coexistence and population genetic structure of the whooper swan Cygnus cygnus and mute swan Cygnus olor in Lithuania and Latvia
Figure 1.
Unrooted statistical parsimony network derived from partial D-loop sequences of whooper swans (Cygnus cygnus) collected in 2010. Circle area is proportional to haplotype frequency. The only detected haplotype of the mute swan (Cygnus olor) is also included in the network. Small circles (positions mv1-mv3) denote inferred intermediate haplotypes and numbers refer to the corresponding sites in the alignment and inferred mutational steps (haplotypes names are indicated in the Table 1).
Species
Sampling area
Parameter of molecular variation n
k
S
H
η
π
K
21 24
1 1
0 0
0 0
0 0
0 0
0 0
Mute swan
Lithuania: Local birds Wintering Total: Lithuania: Local birds Migrating
45
1
0
0
0
0
0
Whooper swan
23 9
11 6
12 9
0.909 (±0.036) 0.917 (±0.073)
13 9
0.0080 0.0087
3.340 3.611
Latvia
15
5
10
0.695 (±0.109)
10
0.0075
3.143
United Kingdom*
4
3
2
0.833 (±0.222)
2
0.0024
1.000
Total
51
17
18
0.879 (±0.032)
19
0.0078
3.256
Table 2.
Molecular variation of mute swans and whooper swans from different sampling areas: sample size (n), number of haplotypes (k), number of polymorphic positions (S), haplotype diversity (H) ± S.D., number of mutations (η), nucleotide diversity (π) and average number of nucleotide differences (K).
*Note: Whooper swans sampled in the United Kingdom in winter were breeders from Iceland
whooper swans is characteristic of wild waterfowl species (Figure 2). Most whooper swan haplotypes attributed to different haplogroups “A” and “B” as defined by unrooted statistical parsimony network analysis were distributed randomly between different sampling sites. A broad-scale distribution of haplotypes indicates that previously isolated populations currently form one panmictic population with clear signs of previous reproductive isolation. Unlike in birds sampled in the Baltic Region, only closely related haplotypes belonging to the more diverse haplogroup “A” 890
were found in birds breeding in Iceland (coded E6C, X4Q, E7D, N6P), whereas haplotypes ascribed to haplogroup “B” were not found in these individuals.
4. Discussion A homogenous genetic population structure was found in mute swans breeding in Lithuania, Latvia, Belarus and Poland. Mute swans breeding in this region are
D. Butkauskas et al.
Figure 2.
The neighbour-joining tree based on partial of D-loop sequences representing phylogenetic relationships of haplotypes, detected among breeding, migrating and wintering whooper swans (Cygnus cygnus) sampled in Lithuania, Latvia and the United Kingdom, and among wintering and migrating mute swans (Cygnus olor) sampled in Lithuania. One haplotype of the tundra swan (Cygnus columbianus, Acc. No. 3A721) and the black swan (Cygnus atratus, Acc. No. FJ379295) obtained from Gene Bank were also included in the construction of neighbour-joining tree for comparison purposes. Numbers on the branches indicate genetic distance between nodes. * Codes of Whooper Swans sampled in Lithuania: birds breeding in Lithuania 7C--, 2H--; migratory birds of unknown origin: 3H--; birds breeding in Poland and sampled in Lithuania: 1R88. Codes of Whooper Swans breeding in Latvia: 1E--, 2E--. Codes of Whooper Swans breeding in Iceland and sampled in the United Kingdom: E6C, X4Q, E7D, N6P. ** Codes of Mute Swans sampled in Lithuania: birds moulting in Lithuania: TU--; birds wintering in Lithuania: 3A5--, 3A8--, 3A9--, 3A7-; birds ringed in Latvia and wintering in Lithuania: EE---, EM503, EK284; birds ringed in Poland and wintering in Lithuania: AC7; birds ringed in Belarus and wintering in Lithuania: AA036, TY42. 891
Coexistence and population genetic structure of the whooper swan Cygnus cygnus and mute swan Cygnus olor in Lithuania and Latvia
likely to be of naturalised origin. Oyler–McCance et al. [44] found relatively low levels of a haplotype diversity in trumpeter swans Cygnus buccinator sampled from in Canada, (Rocky Mountain population, 0.636) and Alaska, North America (Pacific population, 0.649) after the analysis of mtDNA 430 bp of the ND6 and 950 bp of the control region. A diverse population genetic structure is characteristic of whooper swans breeding in Lithuania and Latvia. The results of genetic analyses and field surveys indicate that the breeding population of this species in this region was recently formed by birds from the core breeding area located in the boreal zone of Europe and by individuals from the newly established populations in the Baltic Region. Boiko and Kampe-Persson [45] suggested a mixed origin of whooper swans breeding in Latvia after analyzing their winter distribution. A similar pattern of breeding range expansion in Lithuania and Latvia was recorded for the tufted duck Aythya fuligula [46]. High gene diversity, reflecting an earlier climate history (during the Quaternary period) and gene flow among populations, has been reported for various bird species [47-50]. Both the mute and whooper swan are highly territorial during the breeding season. Pairs of mute swans typically protect their nesting territory both from conspecifics and from other wildfowl species [51]. Pairs of whooper swan protect their nest site and the area around it against conspecifics and are also aggressive towards other species of wildfowl, including the mute swan and Bewick’s swan Cygnus columbianus bewickii [7,52-55]. The whooper swan breeds almost exclusively in natural wetlands (mires, lakes, coastal wetlands, etc.) in the main part of its distribution range located in the boreal zone of Europe [52,56-60]. However, in Lithuania and Latvia, preferred nesting habitats of the whooper wan were found in man-made habitats, particularly fishponds. Fishponds and other man-made habitats are also the preferred breeding habitats of mute swans. These habitats are likely preferred by both swan species in this region due to their almost unlimited food sources.
In fishponds, the feed used for fish cultivation forms the major part of the swan diet [33]. The restricted public access of these artificial wetlands also provide favourable conditions for swan broods, as the impact of human disturbance in fishponds is less significant than in other wetlands. In Lithuania and Latvia, whooper swans are gradually replacing mute swans in these optimum habitats. During the last few decades, whooper swans have also replaced mute swans in many sites in Sweden [54,55]. Several cases have been recorded where mute swans were killed by males or pairs of whooper swans during territorial encounters [55]. Arvidsson [54] suggested that mute swans may eventually be restricted to the coastal wetlands of Sweden, with optimum inland sites being occupied exclusively by whooper swans. The marked differences in population genetic structure of both species found in this study may partly explain the dominance of the whooper swan. Gene diversity is the raw material upon which natural selection can operate [61] and positively correlates with population fitness [62]. The combined effect of both, gene diversity and population fitness, increases the probablility of successful niche expansions and the survival of the species in new environments [63]. If habitat choice is a genetically-determined trait as has been suggested [64], and if mute swans have a genetic preference for the same or similar habitats as whooper swans, interspecific competition between these species in the future could result in a decline in the number of mute swans in their optimum habitats in the Baltic region.
Acknowledgements This study was funded by the Lithuanian Science Council project Nr. LEK-08/2010. The authors are grateful to Dr. Eileen Rees of the Wildfowl and Wetlands Trust in the United Kingdom for samples of whooper swan feathers used for genetic analysis in this study. We thank two anonymus reviewers for their detailed comments and editing on an earlier version of this manuscript.
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