insights to the diversity and history of baltic biota from ......väinölä: diversity and history...

Väinölä: Diversity and history of Balticbiota 1

Insights to the diversity and history ofBaltic biota from molecular data

Revised biogeography of the Baltic Sea

Risto VäinöläUH, Finnish Museum of Natural History Luomus

Zoology Unit

Outline0. Diversity and origins of Baltic biota

conventional view: poor, well known, sum of invasion waves?

New insights from molecular characters

1. More species and stocks: cryptic diversity(Mysis, Marenzelleria, Hediste, Palaemon)

2. East vs West: contact zone of refugial freshwater stocks(sculpin fishes, salmon, grayling, perch, amphipods)

3. Pacific and trans-Atlantic elements, repeated invasion waves(blue mussel, Baltic clam, sturgeon)

4. Rapid speciation and adaptation(hybrid zones and swarms – synthetic diversity, clonality, ecological speciation)

5. Next generation (current generation)– population genomics and genetic basis of adaptation


Identification of environmental problems ?

Risk analysis ? (!)

WP: Risk Analysis:

• risk assessment• what can happen (risks), probability, cost• risk characterization• risk communication• risk management• policy relating to risk

• risk: loss of unique Baltic diversity (species/lineages/locally adaptedpopulations).

• causes: climate change, pollution/eutrophication; (oil) spills,exploitation; habitat destruction; replacement by invading species;hybridization and loss of identity

• ”cost”:- loss/change in ecosystem functions [seldom not due to a single sp.]- loss of unique diversity (a value per se)~ loss of (evolutionary) heritage at different temporal scales

Key issue: how to put value on species and genetic diversity –in terms of the historical and evolutionary processes that created thatdiversity?

cf. valuing cultural or societal heritage


0. Diversity and origins of Baltic fauna:Who do live here, and why?

After the ice ages – everyone is an invader

Species composition determined by

(1) environment: brackish water, boreal climate, ...

(2) opportunities for dispersal / dispersal history

Salinity

Spec

ies

num

berBrackish basin: (non)sea + (non)lake

1/5 of ocean salinity

Species number much smaller fraction

Composition of fauna: ”basic facts"E.g. bivalve molluscs (simpukat):North Sea >150 spp.N Baltic Sea 5 spp. = 3 % of diversity

Several major taxa absent- corals- sea stars (benthic predators)- sea urchins (merisiilit)- cephalopods (mustekalat)- crabs (taskuravut)

Lacking habitats- deep waters- intertidal zone

Suolaisuus

Lajim

äärä


Melting potMixture of faunal elements

• marine• freshwater• invading spp.

(NIS)

Biogeographical elementsA. MARINE SPECIESa1. Most tolerant of Atlantic taxaa2. Arctic marine taxaa3. True brackishwater taxa (estuarine)

a1. Most tolerant of Atlantic taxa

.

- e.g Mytilus (sinisimpukka), Macoma (liejusimpukka)

- typically wide-sprectum intertidal species

- also Gadus (cod), Platichthys (flounder),

Clupea (herring / silakka)

turska

Fucus (rakkolevä)


A. MARINE SPECIES

a2. Arctic marine species (arctic relicts)Absent from the North Sea

e.g. ringed seal, Halicryptus (makkaramato)

Pontoporeia (merivalkokatka)

a3. True brackishwater taxaNorth Sea estuaries and lagoonse.g. lagoon cockle, E. crustulentaidänsydänsimpukka, levärupi

Biogeographical elements

B. FRESHWATER SPECIES

b1. European freshwater taxae.g. pike, perch, pikeperch, roach, lymnaeid snails, Asellus (vesisiira)

b2. ”glacial relicts” – from ice-marginal lakes – now deepwatere.g. Monoporeia, Saduria, Mysis (valkokatka, kilkki, jäännemassiaiset)

Biogeographical elements


Baltic Sea: A new habitat, where species evolved to verydifferent environments meet, at margins of their tolerance

A- Submerged intertidal of ocean shore- Remnant of previous arctic sea- Large estuary of the NE Atlantic (brackishwater taxa)

B- A northern lake (littoral reeds)- A deep northern lakei (cf. Ladoga, Michigan)

C- Invasion route for Ponto-Caspian immigrants

Old and new invasion waves:Baltic colonisation history I

A. Baltic Ica Lake (15 –11.6 kya) - coldwater lake taxaB. Yoldia stage (11.6-10.8 kya) - relicts of the Arctic SeaC. Ancylu Lake (10.8 - 9 kya) - temperate lake taxaD. Littorina Sea (9 - 3 kya) - true marine and brackishwater taxa

Original invasion waves from the neighbouring regions

Diversity of species surviving till now is low


New wave: brackishwater taxa from distantseas gain access to the Baltic

From the Ponto-Caspian (Black/Azov/Caspian Seas):Zebra mussel Dreissena Cercopagis water flea (1990s)

(1800s / 1990s)

From Americas- Marenzelleria spp. 1980sl

- Amphibalanus 1840s- Mya arenaria 1500s ?

round goby(mustatäplätokko)

21st century arrivals in Finland

Tiikerikatka

Gammarus tigrinus

Liejutaskurapu

Rhithropanopeus harrisii

N AmericaàW Europeà S BalticKuvat: Packalen / Peura / SYKE

Sirokatkarapu

Palaemon elegans


New taxa and new functions to the Baltic: GLOBALISATION

- local diversity increases (often)- unique faunal assemblages are lost

most invaders strongly differ from original taxa– in appearance and in ecological function

sp. IV

sp. II sp. I

sp. III

Levels of diversity:species diversity of widespread taxa is often poorly known(externally similar sibling species)è cryptic invasions

Traditionally, dispersalhistory was inferredfrom geographicalcomparisons of faunas

Mysis (opossum shrimps/massiäyriäiset)


But:Traditional morphological characters often fail to distinguishspecies that diverged in the Pleistocene (too short timeframe) :

Molecular characters = DNA and proteins, 1980sà:more accurate information on species histories

As a rule, DNA-data have changed the concepts of speciesnumbers and of dispersal histories

NEW BIOGEOGRAPHY

Traditionally, dispersal history was inferred from geographicalcomparisons of faunal composition

Molecular characters (species history < 5 Myr)

Evol.age

Evol. tree/taxonomy

Populationhistory

hybridisation

mtDNA–sequences (matrilines) + + + ( - )Nuclear genes

genotyping(microsatst, SNPs)

- ( - ) + ( + )

nuclear gene sequences/RFLPs ( - ) ( + ) - +

proteins (allozymes) ( + ) + + +

”conventional tools”

Next generation - population genomics :

Tens of thousands of markers through the genome; recognition ofgenes related to adaptation


species I species II

Molecular revisions of Baltic taxa I

Mysis relicta sensu lato• jäännemassiaiset / opossum shrimps• dominant pelagic crustaceans• ”glacial relict” (circumpolar lakes)

Molecular data (allozymes, 1986) :

Two distinct species in Nordiclakes and the Baltic Sea- several indipendent gene markers = characters- sympatric and allopatric populations- lakes isolated > 10 000 years- reproductive isolationè biological species

- F1 hybrids 0.5 %

- molecular clock: age >1 million yr (cf. 10 000)

IIIII

IVSt. LawrenceChesapeakeBay

NorthSeaNORWAYBalticSeaI

Ma coma balthica

Initial data set (N =251; 96%)allopatric populations:

lakes

Baltic Sea

Test data set (N =204; 91%)

allopatric

sympatric

species I

species I

species II

species II

20

20

20

20

10

10

10

10

N

(seven variables)(Väinölä et al. 2002)

Multivariate morphometric analysis corroborated thespecies boundaries initially found by molecules


Progress in systematics: species discovery1984molelcular description 1986

closer characterisation of Baltic distributions 1998morphometric charaterisation 2002

+ DNA, qualitativemorphology, circum-polarmapping…

Formal taxonomicdescription of new spp.Based on molecules andmorphology in 2005

. . .

Mysisdiluviana

Mysis relicta

Mysis segerstralei

Mysis relicta species groupCorrect scale of study: of a circum-polar species complex

Mysis salemaai

Both Baltic taxa are endemicto Northern Europe, but stillof ancient origin

(Audzijonyte & Väinölä 2005)


(morphologically similar sister species) è cryptic invasions

Liejuputkimato Marenzelleria (Polychaeta)

• ”American invader”, appeared in the North Sea 1979, in the Baltic 1985• Molecular data: two distinct species, invaded simultaneously from N

America (Röhner ym. 1996):• Not distinguished previously

even in the native region

A parallel example from the invasive fauna

1985

1979

Cryptic invasions:

• Actually three species in North America, M. viridis, M. virens and a newspecies Marenzelleria neglecta Sikorski & Bick, 2004

• Stíll another invader since appeared in the Baltic, the Arctic M. arctica


Liejuputkimadot Marenzelleria:

M. viridis, M. neglecta, M. arctia- three invasions, almost simultaneus

All present on Finnish coasts

Blank, Laine, Bastrop 2008

M. viridisM. neglectaM. arctia

Common ragworm Hediste diversicolor(merisukasjalkainen)

- Common in shallow-water Baltic, was ”always” here- Common in European estuaries (brackishwater element)

Protein + mtDNA characters:

Two species in the Baltic(species A, species B)

Sympatric in the Gulf of Finland,Bothnian Sea only sp. A.

(4 nuclear markers; no hybrids)

No clear habitat differences; bothpresent also in the North Sea.

No morphological differences known

Röhner ym. 1999 Mar Biol, Audzijonyte ym. 2008 Mar Biol

AB


Hediste cf. diversicolor(merisukasjalkaiset)

mtDNA :In Europe 5-6 distinct evolutionarylineages

Three of those in the Baltic(species A, species B1, B2)

A1 W Europe, BalticA2 Portugal, Morocco

B1 W Mediterranean, BalticB2 Black Sea, Caspian, BalticB3 Adriatic Sea (C Mediterranean)

Virgilio ym. 2009 Mol. Ecol.

A1

B1B2

B3

A2

Balticnuclear marker data:A1 < > B1+B2 Overlap: No interbreeding

B1 < > B2 Contact in Estonia:Probable interbreeding

mtDNA data:A1: high genetic diversity (old & stable)B1+ B2 : low diversity: few invading haplotypes

A1

B1

B2Merisukasjalkaiset


Ragworm Hediste cf. diversicolor

Interpretaton (hypothesis):

A1 : Original in the Baltic and inWestern Europe (since Littorina age)

B1 W MediterraneanB2 Black Sea

These two lineages of the otherspecies B invaded the Baltic later, andnow co-occur with the original speciesA. They are dominant in the S Baltic.

Cryptic invasions, in parallel withsurviving original species.

Ponto-Caspian +Atlantic

A1

B1B2

B3

A2

Kontula, Väinölä 2001;mtDNA+allozymes

• A European freshwater fish, early colonization of Fennoscandia• Also inhabits N Baltic littoral waters (unique in brackishwater)• Western and Eastern races (”C. gobio, C. koshewnikovi”)

Koli 1969, morphometry


mtDNA-lineagesDiagnostic character

2. Mixing of eastern and western freshwater lineages

Bullhead Cottus gobio (kivisimppu)



• Arrived along coastlines in Ancylus time 10 000 ya, was isolated in lakes• Ancient eastern and western lineages survive in lakes and remain distinct

2. Mixing of eastern and western freshwater lineages

Bullhead Cottus gobio

Koli 1969, morphometry


In the Baltic, the lineages later mixed toform a hybrid stock:

new kind of diversity arose in the Baltic,

as a synthesis of existing old diversity

2.2.

Atlantic salmon in the Baltic Sea,genetic data on invasion history(hypoteesi I: Koljonen ym. 1999)

Main genetic subdivision and invasion history1. From eastern ice lakes to southern rivers,Baltic Ice Lake stage2. From the Atlantic to the Yoldia Sea, and thelater deglaciated Bothnian Sea

[ + new data, new hypotheses]


Northern freshwater taxaOn the borderline of the West and East:Secondary contact of distant races/lineages after the Ice Ages- in the Baltic, and in lakes

Melting pot: new kind of diversity from old ingredients in a novel environment

Further Baltic contacts ofWest and East

• Grayling - harjus• Salmon - lohi• Perch - ahven• Ninespine stickleback

- kymmenpiikki0.1

P-AmerikkaSiperia itäinen

läntinen

Kivisimppu / bullheadCottus gobio

Järvikatka / freshwater amphipodGammarus lacustris

Mytilus blue mussel sinisimpukkaMacoma Baltic clam liejusimpukka

Molecular data::

North Sea <> Balticdifferent species (subspecies)

diverged millions of years ago(lineage 200-300 x Baltic age)

Macoma

allotsyymit – Väinölä & Hvilsom 1991, Väinölä & Varvio 1989)

3. Pacific element and repeated waves of invasion

Dominant benthic species in the Baltic (by biomass):


Cryptic invasions in Marenzelleria

Two cryptic species arrived from America, + a third one from the Arctic

To compare:

1985

1979

Pacific mussels in the Baltic Sea

edulis trossulus gallo-provincialis

North Pacific

Baltic

NW Atlantic

North

Atlantic

temperate:

S Europe

à cosmo-politan

Basic divsion Atlantic <> Pacific

atlantinsinisimpukkatyynenmerensinisimpukkavälimerensinisimpukka

M. trossulusM. galloprovincialis

Mytilus edulis

Muodollinen lajikuvaus geenituntomerkkien perusteellaMcDonald & Koehn 1988

complex

Barents SeaNorth Sea

Baltic Sea

White Sea

NE PacificCanadian Maritimes

South Europe ( + California...)

Pleistocene

reinvasio

n(s)

Seconda

rycon

tacts

(&intro

gression, Holoce

ne)

(120 kya?)

Plioc

ene

Pacific

-->Atla

ntic

invas

ions

NW Atlantic

(Trans-Atla

ntic

isolation?)

M. edulis

M. trossulus

Mytilus edulis

Pacific stem lineage

marogeographical context – part of a circumpolar species complex:


ArcticOcean

NW Atlantic

NE Atlantic

North Pacific

Balti

cSe

a

M. petalum Macoma balthica rubra

Macoma balthica balthica

I

IIIIV

II

Macoma petalum

Barents SeaWales, North SeaVarangerfjorden

Baltic SeaWhite SeaNE Pacific

Quebec

Chesapeake Bay ( + California...)

complex

Macoma balthica

Baltic clam Macoma balthica (= Limecola balthica)

again: A Pacific lineageinhabits the Baltic and White Seas

Väinölä 2003 Mar Biol, Nikula ym. 2007 Evolution

subspecies M. b. rubra M. b. balthica

allozymes

M. b. balthica

M. b. rubra

mtDNAM. petalum

Atlantic and Pacific bivalves evolved in isolation for ca 2 Myr(Pleistocene), and diverged genetically (and ecologically), but notin visible characters

When did the different lineages arrive in Europe?What happens when the diverged lineages meet?

Mya Macoma Mytilus

BACKGROUND


Beringian crossroads and Pacific invaders:Great Trans-Arctic Interchange 3.5 Mya

- A major part of the current Atlantic littoral species arrived from the Pacificthrough the Bering Strait:

- littoral bivalves and snails, kelps (brown algae), Zostera, sea urchins- counter-direction e.g. seals, walrus, cod

Mya Macoma Mytilus

Faunal evolution – a deeper perspective:

North Atlantic and Pacific, isolated through the Miocene >5 Mya

Pleistocene – repeated glaciations( > 20 glacial cycles over 2 million years)

• Atlantic ja Pacific mainly isolated(decreased sea levels, harsh climate)

à independent evolution of boreal taxa(sister species, e.g. Atlantic vs. Pacific cod and herring species)

Divergence of Mytilus and Macoma species/ subspecies (bivalves)

Nothing survived in the Baltic (tabula rasa)


Macoma - Repeated invasions of a Pacific stem lineageto both coasts of the Atlantic

When ?

First wave to Europe 2-3.5 Myr ago

Nikula 2008How about the following ones (Baltic, White Sea, Newfoundland):100 000 ya (interglacial), 5000 ya (Litorina warmth), < 500 ya (human)

mtDNA

Baltic Sea hybrid swarm

NE Atlantic

NW Atlantic

N Paci?cN Paci?c

Macoma - Repeated invasions of a Pacific stem lineageto both coasts of the Atlantic

mtDNA-analysis:latest trans-Arctic invasion early post-glacial (< 10 000 yr)Baltic + White/Barents Seas before human influence

Nikula 2008


NE Atlantic

NW Atlantic

N Paci?cN Paci?c

mtDNA


After the ice age, parts of the Atlantic marginal seas were colonizedby Pacific bivalves – parts by ”original” Atlantic ones

Baltic, White & Barents Seas and Canadian maritimes: crypticinvasions and cryptic diversity, that used to be masked by externalsimilarity

(Mytilus trossulus,Macoma. balthica s.str.)

complex

Barents SeaNorth Sea

Baltic Sea

White Sea

NE PacificCanadian Maritimes

South Europe ( + California...)

Pleistoce

ne

reinvas

ion(s)

Secondary

conta

cts

(&intro

gressio

n, Holocene)

(120 kya?)

Plioce

ne

Pacific

-->Atla

ntic

invasio

ns

NW Atlantic

(Tra

ns-A

tlantic

isolat

ion?)

M. edulis

M. trossulus

Mytilus edulis

Pacific stem lineage

ArcticOcean

NW Atlantic

NE Atlantic

North Pacific

Balti

cSe

a

M. petalum Macoma balthica rubra

Macoma balthica balthica

Secondary contact of long-isolated lineages in the Atlantic andBaltic:

What is the outcome? (reproductive isolation, or gene flow)


NE Atlantic

NW Atlantic

N Paci?cN Paci?c


34

3330

253226

29

142131

16246

20179

8193

5

184

1015

28222723

43

36 37

19

3544

10 1220

1811

23

222115

16

PureNE Pacific

”BALTHICA”Rb

PureNE Atlantic”RUBRA”

4124

38

27242825402632

29 39

Murmanswarm

White/PechoraSea swarm

Baltic Seaswarm

0 1 2-1-2

0

1

2

3

-1

-2

PC 1 (64 %)

PC2

( 15

%)

Murman coast

White SeaPechora Sea

Baltic Sea Proper

Danish StraitsSouthern Baltic

Geographicallocation

Danish Straits:North Sea - Baltictransition zone

15

7

89 2

Nuclear gene analysis(allozymes, Macoma):

àHybridization andamalgamation of the divergedstocks

à Genetically unique mixedstocks in European marginalseas

ArcticOcean

NE Atlantic

Pacific

Balti

cSe

a

Macoma balthica

Murman

Baltic

White

Straits

34

3330

253226

29

142131

16246

20179

8193

5

184

1015

28222723

43

36 37

19

3544

10 1220

1811

23

222115

16

PureNE Pacific

”BALTHICA”Rb

PureNE Atlantic”RUBRA”

4124

38

27242825402632

29 39

Murmanswarm

White/PechoraSea swarm

Baltic Seaswarm

0 1 2-1-2

0

1

2

3

-1

-2

PC 1 (64 %)

PC2

( 15

%)

Murman coast

White SeaPechora Sea

Baltic Sea Proper

Danish StraitsSouthern Baltic

Geographicallocation

Danish Straits:North Sea - Baltictransition zone

15

7

89 2

Geneetic amalgamation(hybrid swarm)

Loss of lineage-specificcharacteristics at all levels

New synthetic diversity(from combined gene pool!)

Effects on the function ofpopulations and ecosystems?

Nuclear gene analysis(allozymes, Macoma):

Contact and hybridization ofAtlantic and Pacific stockscreated genetically uniquemixed stocks in the marginalseas

ArcticOcean

NE Atlantic

Pacific

Balti

cS

ea

M. petalum Macoma balthica

balthica


Mixing of old freshwater lineages in the Balticànew kind of diversity generated

cf. previous case:

Cottus gobio kivisimppu

North Sea Straits Baltic

Mytilus edulis

The Baltic blue mussel also represents a mix of Pacific and Atlantic species(hybrid swarm), but with a stromg Mytilus trossulus –prevalence

Different characters (different parts of genome) are differentially mixed

M. trossulus


The two most important benthic taxa in North European marginal seas:

- previously unknown diversity ("cryptic species")- unnoticed invasions, replacing original taxa?

- unique species / races in the European context

- amalgamation of different genetic proveniencesà original genetic identity lost, but

à enlarged genetic basis (gene pool)adaptation to marginal environmentsinstant speciation !!

(cf. dogma – no endemism)

Macoma

Perspectives / prospectsGenomic perspective: different parts of the genome (organelles /crhomosomes / genes) are mixing at different rates:

à genes responsible for reproductive isolation(affected by natural selection against hybrids

à genes related to adaptation to extremeenvironments (brarcish & coldwater)

- how common are such cryptic lineages amongother taxa?

Newer data: next invasion wave:

M. trossulus has also colonized Norwegianand North Russian harbours:

Will the Baltic mixing history be repeated?Väinölä, Strelkov, 2011

x


Sturgeon (sampi) extirpated from theBaltic in the 1900s.

Euroopean sturgeon A. sturio survivesin the Gironde river.

Museum and archeological sturgeonsof the Baltic region (50-2000 ya)however represent another speciesthe N American Atlantic sturgeon(sinisampi), estimated arrival > 4000ya.

à restocking to the Baltic byCanadian stocks, not European !

Sturgeon in the Baltic Sea – another trans-Atlantic invader

Acipenser oxyrinchus Acipenser sturio

Ludwig ym. Nature 2002, BMC Evol Biol 2008Popovic ym. J Biogeogr 2014

Itämeren sinisammen lähtöalueThe region of origin North Americacan be identified, since Americanpopulations are stronglydifferentiated from each other(nuclear gene markers)

Based on analysis of archeologicalsamples from Northern Germany.

Baltic sturgeon (sinisampi)

Ludwig ym, BMC Evol Biol 2008


Baltic sturgeon: evidence from earlier geneleakage, but much less than in the bivalves(c. 5 %)

Ludwig ym, BMC Evol Biol 2008, Popovic ym, J Biogeogr 2014

Instant speciation 2 ?

A narrow-thallus mophotype of the bladder wrack,reproduces mainly clonally in the Bothnian Sea

Fucus radicans ß Fucus vesiculosus

Described formally as a distinct species,pikkuhauru, in 2005

Genetically differs no more than differentF. vesiculosus populations among themselves

Estimate: Fucus radicans arose locally just400 years ago !

”Freezing of an adapted genotype by cloning”?

Bergström ym 2005 J Phycol, Pereyra ym 2009 BMC Evol Biol


Fucus radicansAsexual & dominant in the Quark

Both species coexist further south in theBothnian Sea and S Gulf of Finland,sexual, but do not interbreed

No diagnostic gene markers, repeated”speciation” ?

Ardehed et al. 2016, PLoS One

however…

FlounderPlatichthys flesus(2017)

Pelagic spawning > 11 PSU original stateDemersal spawning < 11 PSU evolved when Baltic first colonized 8.5 kya(in allo/parapatry)

”Pelagic spawners invaded later (Litorina time) but do no more interbreed:several genes show reproductive isolation despite co-occurrence.Ecological speciation inferred.”

Instant speciation 3


Three pathways to fast adaptation andendemism in the Baltic Sea ?

1. Speciation by synthesis- mixing of the gene pools of differentlineages/speciesà wide material for naturalselection to work towards adaptation and genecombination in marginal environment(molluscs, fishes)

2. Freezing of an adapted genotype byclonal reproduction(Fucus: narrow genetic basis, typical plant strategy)

3. Ecological speciation facilitated by temporaryallopatry (flounder)

Next generation -Population genomics

Tens of thousand marker genesthrough the genome

To identify those genes actuallyimportant for adaptation

herringcodsalmonthreespine sticklebackflounder

Kolmipiikki deFaveri ym 2013

insights to the diversity and history of baltic biota from ......väinölä: diversity and history...

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