Download Sympatric speciation in Baltic Sea Fucus populations

Sympatric speciation in Baltic Sea
Fucus populations
Is vegetative reproduction the key for evolution of F. radicans ?
by
Dan Tiderman
Plants & Ecology
Plant Ecology
Department of Botany
Stockholm University
2009/7
Sympatric speciation in Baltic Sea
Fucus populations
Is vegetative reproduction the key for evolution of F. radicans ?
by
Dan Tiderman
Supervisors:
Helena Forslund and Lena Kautsky
Plants & Ecology
Plant Ecology
Department of Botany
Stockholm University
2009/7
Plants & Ecology
Plant Ecology
Department of Botany
Stockholm University
S-106 91 Stockholm
Sweden
© Plant Ecology
ISSN 1651-9248
Printed by Solna Printcenter
Cover: Adventitious branch from Fucus radicans. Photo by Dan Tiderman.
Summary
Speciation processes are a disputed area of research, and subjected to constant review and
adjustment. The theories of allopatric speciation that are focusing on isolation mechanisms as
the dominating force for speciation have been regarded as the main path for speciation, but
have recently been challenged by several studies indicating different modes of sympatric
speciation. Few of these studies have concerned plants, but a recent identification of the Baltic
Sea seaweed Fucus radicans have highlighted a situation of probable sympatric speciation
under some intricate circumstances. The complex history and environment of the brackish
Baltic Sea area, and the predominant vegetative reproduction strategy of Swedish F. radicans
raises several questions. The evolutionary forces present while F. radicans arguably split
from the sympatric populations of Fucus vesiculosus seems ambiguous in several ways and
the evolutionary history is difficult to access. To improve the insight of the domain, a
comparative test of Swedish F. radicans abilities for vegetative reproduction was performed
with the aim to possibly find the forces trigging the emergence of F. radicans and the factors
restricting the current spatial occurrence of this species. Adventitious branches from four
different categories of origin/species from Swedish and Estonian F. vesiculosus and F.
radicans respectively were compared in a controlled experimental setup to evaluate possible
adaptations towards vegetative reproduction.
The results indicate that the vegetatively reproducing Swedish F. radicans have adapted to
develop more extensive branching and some other morphological traits possibly linked to
nutrient uptake. The observed differences in morphology, the vegetative reproduction
strategy, and the adaptations revealed in this study are proposed to be linked to the northern
boundary of the fundamental niche of these two closely related Fucus species, where the low
salinity environment probably is restricting the success of sexual reproduction. However,
other factors than the reproductive strategy could as well have been triggering the emergence
of F. radicans. When trying to explain the evolutionary history of F. radicans several
scenarios such as polyploidy or relict populations may be suggested as the source for the
emergence of F. radicans in the Baltic Sea. Those are briefly presented and discussed as
alternative explanations, but the complexity of the ecologically related adaptations needs
further both genetic and ecological studies.
3
Sammanfattning
Artbildningsprocesser är ett omtvistat forskningsområde som ständigt är föremål för
uppdateringar och justeringar. De alloptriska artbildningsteorierna som grundar sig på teorier
om att olika former av isolering mellan populationer är den avgörande faktorn för artbildning
har länge varit dominerande. Men de har på senare tid utmanats av studier som påvisat olika
typer av sympatrisk artbildning. Få av dessa studier har emellertid baserats på växtstudier,
men en nyligen identifierad tångart i Östersjön har lyft fram ett fall av trolig sympatrisk
artbildning under något speciella förhållanden. Den komplicerade evolutionära historien och
miljön
i
Östersjöns
brackvattenmiljö,
samt
den
huvudsakligen
vegetativa
reproduktionsstrategin hos de svenska populationerna av den nyligen identifierade arten
Fucus radicans, lyfter fram ett flertal frågeställningar. De evolutionära drivkrafterna som
verkat då F. radicans förmodat uppstått ur Fucus vesiculosus kan uppfattas som mångtydiga
på många sätt och den evolutionära utvecklingen är svår att överblicka. För att skapa mer
förståelse inom området, gjordes en jämförande studie av svensk F. radicans förmåga till
vegetativ förökning med syftet att om möjligt belysa de drivkrafter som legat bakom
uppkomsten av F. radicans samt vilka faktorer som reglerar artens nuvarande utbredning.
Adventivgrenar från fyra kategorier av art/ursprung med svensk och estnisk F. radicans
respektive F. vesiculosus jämfördes i en kontrollerad försöksmiljö för att utvärdera möjliga
anpassningar mot vegetativ reproduktion.
Resultaten påvisar att den vegetativt reproducerande svenska F. radicans har anpassat sig
genom ett mer förgrenat växtsätt samt andra morphologiska egenskaper som möjligen är
förknippade med näringsupptag. De observerade morfologiska skillnaderna, den vegetativa
reproduktionsstrategin och anpassningarna som påvisas i denna studie föreslås vara kopplade
till den nordliga utbredningsgränsen för de två nära besläktade Fucus arterna där den låga
salthalten förmodligen begränsar framgången av sexuell förökning. Det kan emellertid finnas
fler orsaker än reproduktionsstrategier som legat bakom uppkomsten av F. radicans i
Östersjön. Dessa alternativa förklaringar är översiktligt presenterade och diskuterade.
Komplexiteten av dessa ekologiskt betingade anpassningar visar på behov av fler studier,
både inom de genetiska och ekologiska forskningsområdena.
4
Introduction
The emergence of new species were long exclusively regarded as the result of genetic drift in
subpopulations separated by some kind of geographic barrier, and the resulting differentiated
populations where commonly classified as separate species if reproductive isolation had
occurred (Mayr 1963; Dobhansky 1970). The definition of species were later on suggested to
comprise populations with uniting attributes such as reproductive period, anatomy and
reproductive behaviour (Templeton 1989; Paterson 1985). This definition included vegetative
reproducing species which were not considered by the definition of reproductive isolation.
Another view of the species concept is the phylogenetic approach (Cracraft 1983), where
species are regarded as populations with a common ancestor and with some new characters
possible to diagnose. Most of these species theories are compromised in that they do not
account for the ever present and ambiguous processes of hybridisation and the situation of
constant ongoing evolutionary processes. This is still an uncomfortable vagueness in the
speciation concepts and was remarked by Buffon already in the 1800th century (Sörman
2007).
Using a simplified spatial approach, speciation can be separated in to allopatric speciation
where isolation factors are the keys and into sympatric speciation, where speciation occurs
without any apparent isolation between populations. The traditional, and still largely
dominating speciation theories that are based on reproductive isolation all fall into the
category of allopatric speciation where the antagonistic forces of spatially dependent
adaptation and gene flow makes up the key mechanism of the evolutionary process. The
sympatric speciation theory is more recent and suggests that in some circumstances speciation
can occur in populations without the presence of separating barriers, typically in recently
colonized or isolated areas that offer a variety of new niches (Schliewen et al. 2001). An
important mechanism in plants but also known in some animals, are speciation by polyploidy,
where characters can change in relative short periods by chromosome multiplication.
Polyploidy is also suggested to be one of the predominant modes of sympatric speciation in
plants due to the large effects on gene regulation (Otto & Whitton 2000).
Several studies have demonstrated sympatric speciation and some examples are:
differentiating to host plant adaptation in flies (Feder et al. 1988), adaptation to different
patterns for sexual selection in African cichlids (Schliewen et al. 2001), and adaptive niche
separation in salmons (Lu & Bernatchez 1999). In plants, however some of these adaptive
5
forces do not seem applicable due to the sessile life strategies in plants which inhibit active
choosing among patchy micro niches and are excluding the impact from active mating.
However recent studies indicates that sympatric speciation has occurred in the Baltic Sea
seaweed, Fucus radicans (L. Bergström et L. Kautsky sp. nov.). The species has arguably
descended from Fucus vesiculosus (L.) (Pereyra et al. 2009) and has recently attracted
attention, as new research has revealed that this dwarf morph is to be regarded as a species of
its own (Bergström et al. 2005).
The scene of this sympatric speciation, the Baltic Sea, is the largest brackish water body in the
world and is intriguing as a scene for speciation processes for several reasons. The
longitudinal extension makes for a varying range of climatic environments. The restricted
influx of marine water to the southwest in conjunction with abundant freshwater supplies
from the northern parts results in a consecutive salinity gradient increasing southwards. The
young and complex evolutionary history of approximately 8000 years since the last
glaciations (Björk 1995) entails a flora and fauna in transformation (Kautsky et al. 1992;
Johannesson & André 2006). The brackish environment generally present a challenging
environment, optimal neither for organisms from marine or freshwater origin. The
composition of the inhabitants today (Sommer et al. 2008; Schmölke 2008) indicates that the
majority of the current marine species immigrated during the marine Littorina Sea period. The
marine organisms in the area have since then been going through an intensive adaptation and
extinction phase (Johannesson & André 2006) in a sequence of successive transformation of
the environment towards freshwater conditions.
The fucoids F. radicans and F. vesiculosus are the only structural large, long-lived macroalgal
species in the Bothnian Sea where they form the canopy along bedrock and gravel shores
making an important foundation for the ecological communities present (Wikström &
Kautsky 2007, Kautsky et al. 1992). Fucus radicans have been found in the Bothnian Sea, and
along the Estonian coast (Bergström et al. 2005; Pereyra et al. 2009). Findings of the species
in the Gulf of Finland are difficult to assess due to uncertainties regarding the wide range of
morphological variance found, which is not yet genetically resolved. Just like F. vesiculosus
the Estonian populations of F. radicans are sexually reproducing. Contrary to this, the F.
radicans populations in the Bothnian Sea are predominantly reproducing vegetatively
(Bergström et al. 2005; Tatarenkov et al. 2005) growing adventitious branches that fall off to
generate new clonal individuals (Tatarenkov et al. 2005). This situation of regional vegetative
6
reproduction may cause low genetic variation and may consequently lead towards long term
restriction in adaption capabilities. This could possibly make the clonal populations
vulnerable to long term changes in the environment (Spielman et al. 2004).
The situation of an apparent sympatric speciation into the current clonal populations raises
several questions. Why and how did the speciation occur and why are clonal F. radicans
populations successful in the Bothnian Sea and especially in the northern parts where studies
indicate that it is relatively more abundant (Forslund 2009a). Could the vegetative
reproduction actually be the key for the emergence of F. radicans ? One possible explanation
is that vegetative reproduction is more effective due to the limited efficiency of sexual
reproduction in low salinity environments, where osmosis mechanisms restrict the success
and survival of the eggs released (Serrão et al. 1996; Serrão et al. 1999). This could possibly
explain why the vegetatively reproducing F. radicans has evolved in this area, at the margin
of the fundamental niche for fucoids. Also, other factors in these marginal areas could be of
importance as environmental stress factors probably are restricting F. vesiculosus in more
ways than just reproduction, thus possibly relieving some of the overall competitive pressure
for F. radicans (Johannesson & André 2006).
One prerequisite for F. radicans to be superior to F. vesiculosus regarding vegetative reproduction is that some new traits enhancing this reproduction strategy have been acquired. I
tested the hypothesis that clonal Fucus populations should use more resources for vegetative
reproduction than sexually reproducing Fucus populations by counting the number of adventtious branches per biomass in plants of both F. vesiculosus and F. radicans from two regions.
The extent, and establishment of released adventitious branches are hypothesised to be more
critical to F. radicans with a reduced ability to establish by sexually produced zygotes. In the
sexually reproducing populations, adventitious branches could possibly serve primary as free
floating individuals improving the ability for long range spreading (Ingólfsson 1995) and thus
be assumed to be of less importance. I tested the establishment ability of adventitious
branches by growing adventitious branches from Estonian and Swedish F. radicans and F.
vesiculosus respectively on a substrate while examining the extent of rhizoid development and
comparing the ability to adhere to the substrate.
7
The following hypothesis where also defined: Adventitious branches from F. radicans have
more cryptostomata than does F. vesiculosus. The rationale for this is that the narrower thallus
in F. radicans (Bergström et al. 2005) allows for less nutrient uptake, which should be
compensated by a higher density of cryptostomata provided with hyaline hairs possibly
serving as a expanded surface for nutrient uptake (Deboer & Whoriskey 1983). This was
tested by counting the cryptostomata in adventitious branches from the two species, grown in
the same environmental conditions.
Material & Methods
Study species
The macroalgae F. radicans, and F. vesiculosus are two of the three known fucoids in the
Baltic Sea. They are both canopy forming in shallow waters and on hard substrate bottoms.
As all fucoids they are perennial and produce one type of diploid thallus.
Fucus radicans differs from F. vesiculosus morphologically in having a more shrubbery
appearance, being smaller in size and slimmer in the dimensions. It also lacks the vesicles
present in F. vesiculosus. Though being dioecious as is F. vesiculosus, the Bothnian Sea
populations of F. radicans is predominantly vegetative reproducing (Tatarenkov et al. 2005),
while the Estonian populations of F. radicans seems to reproduce predominantly sexually like
F. vesiculosus (H. Forslund pers. comm.). The adventitious branches growing from the thallus
are the main source for vegetative reproduction in both F. radicans and F. vesiculosus. These
branches can remain on the thallus extending the branching or detach to serve as propagules
for new individuals. If the rhizoids originating from the base of the adventitious branches,
find a suitable substratum, the branch has the possibility to attach and establish a new sessile
plant (Tatarenkov et al. 2005).
Study sites and sampling
Individuals from four different combinations of population sites and species where used for
the study. Swedish and Estonian F. radicans and Swedish and Estonian F. vesiculosus. The
Swedish individuals of both F. radicans and F. vesiculosus where collected in Öregrund the
24th of April and the Estonian plants at Ösel on the 1st of Maj. The plants where transported in
cool and humid conditions and placed in tanks after 1-2 days and subsequently accommodated
on the bottom of shallow water open cisterns for a period of 7-8 weeks at the Askö marine
laboratory. The cisterns where supplied by continuous incoming sea water with an
approximate temperature of 14ºC and 6.5 ‰ salinity and natural light. From each of the
8
site/species combinations, 10 plants and a couple of reserve plants where randomly picked. It
should be noted that in collecting the Estonian samples of F. vesiculosus some plants where
short in adventitious branches. In these cases a new plant where randomly choosen. Also
notably is that the Estonian samples of F. vesiculosus by visual impression where in slightly
worse condition than the other categories sampled. The number of adventitious branches for
each plant where counted and the plants where weighted wet after surplus water was removed.
Ten adventitious branches of 2-5mm in size were detached from each sample plant and
located on granite discs of 35mm diameter. The discs were encircled by a cylindrical mesh net
of 40mm height attached to the discs perimeter by aquarium silicone. The net served as a
restricting barrier in case of turbulence or accidental movements of the samples. The samples
were placed in a temperature of 15ºC inside oblong plastic containers of approximately 80
liter and a water depth of 75mm. The system was continuously fed by sea water in an
approximately rate of 30 l/h with a temperature of 14ºC. The sample discs where randomly
orientated 35 mm below the surface in the drain end of the container. The water were mixed
by air feeding stones in the tap end of the container causing slight surface undulations in the
drain end. Illumination of 3200 Kelvin color temperature were present for 18 hours/day with
an intensity of 87 µmol s-¹ m² at surface level. Gentle cleaning of the mesh net were executed
at an interval of 4 weeks approximately. After 11 weeks the adventitious branch samples were
examined visually using magnification equipment. The observations made were: occurrence
of rhizoids, if rhizoids where attaching to the disc, the amount of growth and the cross section
shape of the thallus, if cryptostomata were present and the amount observed. The observations
were either boolean or ordered classifications based on definitions as follows:
Definitions and classification for observations:
Occurrence of rhizoids – rhizoids visible or not visible
Rhizoids attached to the substrate – The base of the branch steadily attached by rhizoids and not detached by
a slightly movement of the branch in the upper part.
The amount of growth –
 No apparent growth
 Limited growth, less than or equal to 50%
 Substantial growth, more than 50%
Cross section shape of main body –
 Circular: width less or equal to 2x the height
 Elliptical: width more than 2x, but less or equal to 3x the height
 Flattened: width more than 3x the height
Amount of cryptostomata –
 No/few: Not visible or less than 4
 Normal :4 or more
9
Statistical analyses of the number of adventitious branches were made using one-way
ANOVA. Occurrence of rhizoid and cryptostomata were analysed by Fisher's Exact Test and
the growth and cross section shape were analyzed by chi-square methods. All analyses were
made using R version 2.9.0 (R Development Core Team 2009).
Results
Number of adventitious branches
The vegetative reproducing Swedish F. radicans had significantly more adventitious branches
than the sexually producing categories (F4, 45 = 86.26, p < 0.001,). Swedish F. vesiculosus also
showed significant more branches than the Estonian counterpart. (F4, 45 = 86.26, p < 0.01).
Figure 1
Number of adventitious branches per g measured wet weight in plants from the
four combinations of species/origin. Error bars show confidence interval (n= 10)
10
Rhizoid development by the adventitious branches
Very few of the adventitious branches developed rhizoids. The results showed no differences
between categories (p = 0.34). Only 7 of the total number of branches used(450) where firmly
attached to the platter.
Figure 2
The percentage of adventitious branches that developed rhizoids showed no significant
differencies between the origin/species combinations [ n = 100(Swedish F. radicans);
120(Estonian F. radicans); 120(Swedish F. vesiculosus); 110(Estonian F. vesiculosus) ]
11
The overall thallus growth and the cross section shape
The Estonian F. radicans had the highest general growth rate with 88% having substantial
growth, (χ² = 120.6; df=6; p<0.001). In the samples of Swedish F. radicans, no single
adventitious branch were classified as having substantial growth (Fig 3). The two different
categories of F. radicans showed generally a growth pattern with rounded cross sections,
whereas the Swedish F. vesiculosus were generally elliptical, (χ² = 432.2; df=6; p<0.001). The
most flattened growth pattern were found in Estonian F. vesiculosus where 54% had a flat
cross section and 38% where elliptical (Fig. 4).
Figure 3
The relative amount of growth for each Fucus category divided into the 3
classifications defined. (n=100,120,120,110 respectively).
Figure 4
A comparison of the cross section shapes for each Fucus category divided into
different flatness classifications of the thallus. (n=100,120,120,110 respectively).
12
The amount of Cryptostomata
Although F. vesiculosus developed less cryptostomata overall than did F. radicans, different
patterns were found depending on the origin. In Sweden F. vesiculosus had more
cryptostomata than F. radicans (p < 0.01) but in Estonia the species-cryptostomata relation
was reversed (Fig. 5).
Figure 5
The results indicate that F. radicans in Estonia had slightly more samples with a
higher amount of cryptostomata compared to the F. vesiculosus populations, but
with the opposite relation found in the populations originating from Sweden
(n=100,120,120,110 respectively)
13
Discussion
The results from this study shows that the vegetative reproducing Swedish F. radicans had
significantly more adventitious branches than the predominantly sexually reproducing
populations of F. vesiculosus and the F. radicans population originating from Estonia. In line
with the hypothesis stipulated, this could indicate that Swedish F. radicans are allocating
more resources into producing vegetative propagules for new individuals instead of investing
efforts in producing sexual gametes. This could imply that the extent of branch development
in Swedish F. radicans may be a result of adaption towards an amount of branch development
that brings a reproductive advantage in the special circumstances of the Bothnian Sea.
Presuming that the majority of adventitious branches produced are not departed from the
source plant and thus brings a more shrubby morphological overall appearance, a second
interpretation of the results is possible. Traits such as extensive branching could potentially be
an advantage in the prevailing conditions by extending the surface area for nutrient uptake
while still keeping an overall size. The more compact morphology could make the plant less
vulnerable to external factors like ice scouring or limitations in nutrient resources. The
extended nutrient uptake capabilities could also imply that the improved vegetative reproductive abilities could be a secondary effect and may be the result of an initial morphological
adaption towards extended surface area. Whether or not any of these adaptive forces were
initially driving the adaption towards a more extensive branching is not clear, but the advantages from both of these consequences may be crucial for the fitness of Swedish F. radicans.
One question arising when analysing the amounts of branching is if the morphological
differences are a case of adaption or plasticity. In the case of the two F. radicans populations,
plasticity could not be excluded due to the fact that the spatially split populations initially had
different environmental conditions, even if the recent environment have been the same. This
would however imply that the plasticity is a trait unique for F. radicans because I) the results
comparing the two different sympatric Fucus species from the Swedish coast also show clear
difference in the amount of branching, II) the spatially split F. vesiculosus population does not
show the same obvious difference in branching as the F. radicans populations.
The test of rhizoid development under artificial conditions showed less overall growth of
rhizoids than expected and no species/origin combination produced more rhizoids than the
others. As shown by the results the overall growth of the adventitious branches were not low
in general. This signs of a basically sound environmental living conditions should
14
consequently rule out the environment to be the cause for the generally meagre rhizoid
development and leads to the suspicion that some key environmental factors controlling
rhizoid growth have been poorly understood, and that the trigger inducing rhizoid
development is still to be found. A previous studie (Tatarenkov et al. 2005) has shown
significant differences between the rhizoid development in F. radicans and F. vesiculosus and
a more extensive rhizoid development overall. If further studies are to be performed,
preparatory work is needed to examine the environmental factors trigging the growth of
rhizoids, provided such factors are to be found. The success rate of vegetative propagules in
natural conditions is another issue of interest for understanding the dynamics of the
evolutionary pathways, this is an area largely yet to be investigated.
To try to answer the question if the vegetative reproduction is the key to the emergence of
sympatric Fucus populations in the Bothnian Sea, it is appropriate to monitor alternative
reasons for the current spatial presence of F. radicans. That is, what are F. radicans merits in
this particular environment compared to its larger sibling species F. vesiculosus? If no
restricting environmental factors are present it is generally a good idea to maximize the
available resources and grow big, as this will enhance the competitive ability in several ways,
as for example suppression of competition or greater reproductive ability. On the other hand if
resources become sparser, predation increases, different forms of environmental stress factors
are present, a bigger body may not be the best solution and could possibly backlash due to
difficulties at maintaining the more abundant biomass and coping with temporary harsher
conditions. This generally mean that for F. radicans there may be more benefits than
reproductive advantage alone to favor the species in the northern Bothnia Sea which is
constituting one of the margins of the fundamental niche for Fucus species. Some
environmental factors for further studies are the physiological impact of regional variations in
seasonal salinity due to river outwash in the north, or the consequences from ice scouring and
the effects of the more extended periods of permanent sea ice in the north.
A puzzling situation is the presence of F. radicans in Estonia. In this area where F. radicans
reproduces sexually the benefits of vegetative reproduction or the possible impact of stress
factors areas are not that obvious. One possible reason for the presence here (L. Kautsky pers.
comm.) is that the sea bed is constituted by coarse gravel over finer sediments. This may be
prohibiting the larger F. vesiculosus from reaching reproductive size. The cause for this could
be that plants of greater size, as F. vesiculosus, established on the relative fine sized gravel is
15
easier moved away by currents or wave action. This is then possibly a lesser problem for the
more slender built F. radicans.
Comparing the two Estonian Fucus species, F. radicans had slightly more cryptostomata than
F. vesiculosus. With the former species having a relatively slimmer thallus cross section,
more cryptostomata and thus more hyaline hairs for nutrient uptake could be a way of
compensating for the relative lesser thallus surface area. However it should be noted that the
greater amount of cryptostomata in this study could be an effect of the overall greater growth
noted in the Estonian F. vesiculosus samples. There could also be a lesser need for surface
area in F. radicans due to the geometric laws stating that a smaller body possesses a greater
surface area to volume quota. Contrary to the Estonian populations the Swedish F. radicans
showed less cryptostomata than the Swedish F. vesiculosus. This is opposing the nutrient
theory proposed for the Estonian populations but could be a logic consequence of the
comparably more shrubby appearance and more extensive branching in Swedish F. radicans
compared to the Estonian counterpart. This shrubbiness could serve as an alternative mean of
extending the surface area.
Then why do not the Swedish populations use the same strategy with more cryptostomata as
the Estonian populations? The reasons could be twofold. Firstly the branching could serve a
vital secondary purpose as extended capacity for vegetative reproduction in the northern low
salinity environment generally hampering sexual reproduction ( Serrão et al. 1996; Serrão et
al. 1999). Secondary, it could be a way of improving the durability against herbivores by
minimizing the hyaline hairs otherwise needed and possibly attractive for herbivores. The
latter would also be in line with the proposal by Forslund (2009b) that Swedish F. radicans
has lower levels of chemical defense than F. vesiculosus which consequently could imply that
F. radicans are more vulnerable to herbivores. By concatenating the results from this study
and the previous discussion of evolutionary forces, a web can be constructed illustrating the
suggested interacting factors and thus possibly explaining the spatial occurrence of Fucus
radicans in the Baltic Sea (Fig 6). In comparing the ability for nutrient uptake in F. radicans
to sympatric populations of F. vesiculosus, it is possible to propose that F. radicans could be
using an alternative strategy for extending the surface area. This strategy may be well suited
to the Bothnian Gulf with implications for reproductive success in the north and to herbivore
defense abilities in the south thus delimiting the population to the current spatial range.
16
Figure 6
Comparing the ability for nutrient uptake in F. radicans to sympatric populations of F. vesiculosus with
the Estonian population to the right and the Swedish to the left, the ability of F. vesiculosus are used
as a reference level on the line indicating the necessary level of nutrient uptake ability. Divergent
abilities from this norm is represented by arrows indicating traits that are positive(up) or
negative(down). Attached are miniatures of the results from this study, supporting the claims for the
deviations in nutrient uptake ability. To the far left are some proposed derived consequences of the
nutrient deviations influencing the spatial occurrence of the Swedish F. radicans. These traits are
suggested to have implications for reproductive success in the north and to herbivore defense abilities
in the south thus limiting the population to the current spatial range.
In contemplating some scenarios describing the sympatric speciation process and especially
emphasizing the impact from the vegetative reproduction strategy used by Swedish F.
radicans, it is probable that a few clonal individuals of F. radicans have succeeded in
populating vast spatial areas (Tatarenkov et al. 2005). This could have been made possible
through exploiting this alternative reproduction strategy and by doing so tweaking the rules of
speciation. This alternative path is realized by effectively displacing sexual reproduction as
the common framework for the speciation processes and thus minimizing the counteracting
forces of hybridization. Maybe these resulting populations are to be regarded as a transitional
form in a temporary abnormal evolutionary situation, with clonal individuals exploiting a
temporary marginal environment to make improved clonal abilities to prosper in a timeframe
17
of limited endurance. The longevity of the genetically restricted populations of clonal F.
radicans will ultimately give the answer.
Even if we are witnessing a turmoil of ongoing speciation processes beginning after the
deglaciation about 8000 years ago, it would be extraordinary to imagine a rapid speciation
with these type of adaption’s realized in a very short time space, even as short as 400 years as
proposed in models by Pereyra et al.(2008) based on microsatellite markers. The parallels to
this would be few worldwide and the tendency for F. radicans populations to emerge in some
different areas of the Baltic Sea under slightly different environmental conditions showing
such minor morphological differences is amazing. Although somewhat improbable there is a
possibility that convergent evolution has occurred in the geographically separated areas of the
Bothnian Sea and of Ösel. Somewhat more probable is an initial evolution in one area and
subsequent spreading and readapting into another. Maybe clonality in the Swedish/Finnish
population is such a secondary trait recently emerging. The high heterozygosity found among
clonal populations (Johanson 2008) could support this. If this trait of clonality commonly
known in marginal areas is indeed a recent evolution we can expect further loss of sexual
reproductive abilities in the future, based on indications that environmental suppression of
sexual recruitment may lead towards sterility (Eckert 2002). Provided these populations of F.
radicans emerged suddenly and maybe even separately, some traits already inherent may
suddenly have prospered perhaps due to a change in the environmental conditions. One
possibility is that a suppressed relict population of F. radicans has been present in the Baltic
Sea. Another possible scenario supported by the fast and simultaneous evolution of the F.
radicans populations and the morphologic relationship between F. vesiculosus and F.
radicans is polyploidy. If a species resembling F. radicans once was the now extinct ancestor
to the current F. vesiculosus we could maybe be witnessing a retreat from polyploidy
triggered by the prevailing environmental conditions. Regardless the specific history, the
evolutionary history of F. radicans is probably a scenario consisting of a mix of punctuated
equilibrium phases and intermediate gradualism where the former pattern have been realized
through evolutionary opportunism in situations of sudden environmental changes.
18
To conclude the experiences from this study, several adaptations of possible importance are
found in the Swedish populations of F. radicans. These adaptations are: the more extensive
branching, the vegetative reproduction, the possibly adapted levels of cryptostomata, and the
morphological traits general to F. radicans. It would probably be unwise to view these
adaptions as singular individual traits, but instead as a web of intricate combined and
coordinated adaptations resulting in populations well suited to the very special marginal
environment of the Bothnian Sea. It is not obvious that vegetative reproduction ability is the
key for the evolution of Fucus radicans, but regardless of whether the clonality was an
original trait and a key for the speciation to occur, or was a secondary adaption and maybe
ultimately an evolutionary dead end, it is very likely to have been of great importance for the
species present success in the Bothnian Sea.
Acknowledgements
Many thanks for the general support to the Plant Ecology people in the department of Botany
at the University of Stockholm. Also thanks to the staff at the Askö Marine Laboratories for
facilitating the practical parts of this work. Very special thanks to my supervisors Helena
Forslund and Lena Kautsky for sharing their knowledge and supporting me with invaluable
guidance and advice.
19
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Carlsson, Lars: Vegetationen på Littejåkkadeltat vid Sitasjaure, Lule Lappmark.
Tapper, Per-Göran: Den maritima lövskogen i Stockholms skärgård.
Forsse, Erik: Vegetationskartans användbarhet vid detaljplanering av
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Bråvander, Lars-Gunnar och Engelmark, Thorbjörn: Botaniska studier vid
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Engström, Peter: Tillväxt, sulfatupptag och omsättning av cellmaterial hos
pelagiska saltvattensbakterier.
Eriksson, Sonja: Vegetationsutvecklingen i Husby-Långhundra de senaste
tvåhundra åren.
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områdets exploatering för vattenkraftsändamål i Ritsemprojektet.
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Vilhelm: Kunskapsöversikt och forskningsbehov rörande mekanisk påverkan på
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Kalvas, Arja: Jämförande studier av Fucus-populationer från Östersjön och
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coastal predators and ecosystems.
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invertebrates and plants.
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survive in-situ?
2007:11 Kolb, Gundula: The effects of cormorants on population dynamics and food web
structure on their nesting islands.
2007:12 Honkakangas, Jessica: Spring succession on shallow rocky shores in northern
Baltic proper.
2008:1 Gunnarsson, Karl: Påverkas Fucus radicans utbredning av Idotea baltica?
2008:2 Fjäder, Mathilda: Anlagda våtmarker i odlingslandskap- Hur påverkas
kärlväxternas diversitet?
2008:3 Schmalholz, Martin: Succession in boreal bryophyte communities – the role of
microtopography and post-harvest bottlenecks.
2008:4 Jokinen, Kirsi: Recolonization patterns of boreal forest vegetation following a
severe flash flood.
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2008:5 Sagerman, Josefin: Effects of macrophyte morphology on the invertebrate fauna in
the Baltic Sea.
2009:1 Andersson, Petter: Quantitative aspects of plant-insect interaction in fragmented
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2009:2 Kolb, Gundula: The effects of cormorants on the plant-arthropod food web on their
nesting islands.
2009:3 Johansson, Veronika: Functional traits and remnant populations in abandoned
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2009: 4 König, Malin: Phenotypic selection on flowering phenology and herbivory in
Cardamine amara.
2009:5 Forslund, Helena: Grazing and the geographical range of seaweeds –
The introduced Fucus evanescens and the newly described Fucus radicans.
2009:6 von Euler, Tove: Local adaptation and life history differentiation in plant
populations.
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