Le mimétisme mullérien chez les papillons: évolution et conséquences d'une innovation majeure

(1)

Marianne Elias

Institut de Systématique et Evolution de la Biodiversité MNHN

Le mimétisme mullérien chez les papillons:

évolution et conséquences d'une innovation majeure

(2)

Fitness = survival x reproduction

not being eaten

(3)

APOSEMATISM:

ADVERTISING DANGER / UNPALATABILITY

(4)

APOSEMATISM:

ADVERTISING DANGER / UNPALATABILITY

(5)

APOSEMATISM:

ADVERTISING DANGER / UNPALATABILITY

= toxic

(6)

Henry Walter Bates, 1862

Palatable species mimic unpalatable aposematic species and are protected from predation.

BATESIAN MIMICRY

(7)

Dentrobate poison frogs

Myrmarachne spider weaver ant

Honey bee Harmless hover fly

Yellowjacket wasp Clearwing moth

Apheloriine millipedes

(8)

Why do multiple unpalatable prey look alike?

(9)

→ reduces per-capita cost of educating predators Fritz Müller, 1879

Unpalatable species are selected to converge in warning pattern → Müllerian mimicry

a₁ a₂

n_k n_k

Species 1 Species 2

MÜLLERIAN MIMICRY

(10)

→ reduces per-capita cost of educating predators

a₁+a₂ n_k

Fritz Muller, 1879

Unpalatable species are selected to converge in warning pattern → Mullerian mimicry

Species 1 Species 2

MÜLLERIAN MIMICRY

(11)

→ reduces per-capita cost of educating predators

a₁+a₂ n_k1

=

a₁n_k/(a₁+a₂)

<n_k

n_k2 =

a₂n_k/(a₁+a₂)

<n_k Fritz Muller, 1879

Unpalatable species are selected to converge in warning pattern → Mullerian mimicry

Species 1 Species 2

Positive interactions!

MÜLLERIAN MIMICRY

(12)

Positive interactions!

MÜLLERIAN MIMICRY

Species 1 Species 2 Species 3 Species 4

(13)

→ mimicry rings

MÜLLERIAN MIMICRY

co-mimics co-mimics

(14)

Heliconius (46 species) Ithomiini (390 species)

● Nymphalidae, Heliconiinae 90 mya ● Nymphalidae, Danainae

● Pan-neotropical ● Pan-neotropical

● Unpalatable, aposematic

→ cyanogenic glucosides ● Unpalatable, aposematic

→ pyrrolizidine alkaloids

=> Müllerian mimicry => Müllerian mimicry

● Evo-devo, genomics ● Ecology, diversification

MULLERIAN MIMETIC BUTTERFLIES

(15)

Heliconius Ithomiini

Genome size

Linkage map Assembled genome

Genes

Transcriptomes

Diversity

Age 380

46mya 18mya

46

Mate-choice bioassays

Local diversity and abundance

+ +++

(16)

OUTLINE

● I- The puzzle of mimicry diversity

● II- Imperfect mimicry

● III- Mimicry as a driver of speciation

● IV- The genetic bases of colour pattern variation

● V- The fabulous story of Heliconius numata

● VI- Mimicry and the evolution of the ecological niche

(17)

THE PUZZLE OF MIMICRY SIGNAL

DIVERSITY

(18)

(19)

DIVERSITY OF MIMICRY PATTERNS?!?

(20)

Among different regions

Within community

Within species within community

Heliconius numata Ithomiini

DIVERSITY OF MIMICRY PATTERNS?!?

(21)

Heliconius

→ Spatial mosaic of patterns

DIVERSITY AMONG REGIONS

(22)

Sherratt 2006, J Theor Biol

spatially explicit individual-based model Lattice with 2 species, m morphs. In each cell:

• Predation or not

• Dispersal

• Reproduction (with mutation)

→ Spatial mosaic of morphs + narrow hybrid zones

DIVERSITY AMONG REGIONS

(23)

Modèles Ithomiini

Mime H. numata

Joron et al. 2001, Evol Ecol

LOCAL DIVERSITY WITHIN SPECIES

Heliconius numata

(24)

LOCAL DIVERSITY WITHIN SPECIES

Tarapoto, Peru

7 forms of Heliconius numata

(25)

espèces modèles espèce mimes

LOCAL DIVERSITY WITHIN SPECIES

(26)

espèces modèles espèce mimes

LOCAL DIVERSITY WITHIN SPECIES

(27)

Joron & Iwasa 2005, J Theor Biol Analytical model

2 patches

• Heterogeneity of mimetic environment (cf. Sherratt 2006)

• Migration of mimetic species

→ Stable polymorphism If strong heterogeneity and mild toxicity

LOCAL DIVERSITY WITHIN SPECIES

(28)

Ithomiini

habitat butterfly predator

microhabitat niche partitioning Ecological heterogeneity =>

Beccaloni 1997, Biol J Lin Soc

De Vries et al. 1999, Biol J Lin Soc

→ ecological segregation of mimicry rings

DIVERSITY WITHIN COMMUNITY

(29)

Stochastic individual-based model

2-dimension ecological space, 10 species, 5 mimicry patterns

• Heterogeneous predation

• Reproduction - mimicry pattern - niche

• 5000 generations 100 runs

homogeneous moderately heterogeneous strongly

heterogeneous

Gompert et al. 2011, J Theor Biol

DIVERSITY WITHIN COMMUNITY

Microhabitat niche value

(30)

homogeneous moderately heterogeneous strongly

heterogeneous

→ Heterogeneous predation promotes diversity

strongly heterog.

moderately heterog.

homog.

NO predation

DIVERSITY WITHIN COMMUNITY

(31)

→ Heterogeneous predation promotes association of mimicry pattern with ecological niche

association

DIVERSITY WITHIN COMMUNITY

strongly heterog.

moderately heterog.

homog.

NO

predation moderately heterog.

homog.

NO predation

(32)

Community Anangu in lowland Ecuador

58 ithomiine spp, 8 mimicry rings 176 bird spp

DIVERSITY WITHIN COMMUNITY

(33)

(34)

(35)

(36)

(37)

0 0.5

1 1.5

2 2.5

m

observed in rope surveys

→ Mimicry rings are segregated by flight height, topography and forest structure

Spot-backed antbird

Golden-headed manakin

→ Predators are segregated by flight height and topography

Willmott et al. in revision

FLIGHT HEIGHT

DIVERSITY WITHIN COMMUNITY

(38)

microhabitat niche partitioning Ecological heterogeneity =>

DIVERSITY WITHIN COMMUNITY

(39)

homogeneous predation

moderately heterogeneous predation

strongly heterogeneous predation

→ stochastic and selective processes can maintain mimicry diversity

Among regionsWithin species within communitywithin community

DIVERSITY OF MIMICRY PATTERNS?!?

(40)

IMPERFECT MIMICRY

(41)

HOW GOOD CAN A MIMIC BE?

● “imperfect mimicry”

- Relaxed selection

- Developmental constraints

- trade-offs (e.g., multiple models)

● potential explanations

(42)

HOW GOOD CAN A MIMIC BE?

Tarapoto, Peru Sampling all mimetic butterflies (2295 specimens)

(43)

HOW GOOD CAN A MIMIC BE?

(44)

HOW GOOD CAN A MIMIC BE?

● Quantifying resemblance: Colour Pattern Modelling (CPM) Colour attribution

Wing alignment Colour segmentation

PCA to summarize pattern variations

Le Poul et al., in prep

(45)

→ Resemblance depends on phylogenetic relatedness among species

→ developmental constraints?

→ Evidence for both strong and relaxed selection

Le Poul et al., in prep

HOW GOOD CAN A MIMIC BE?

(46)

MIMICRY AS A DRIVER OF SPECIATION

(47)

MIMICRY AS A DRIVER OF SPECIATION

1 species 2 species

Divergence

Reproductive isolation

- +

Speciation = evolution of reproductive isolation

(48)

MIMICRY AS A DRIVER OF SPECIATION

Ecological speciation: speciation driven by divergent selection

e.g., phytophagous insects

(49)

MIMICRY AS A DRIVER OF SPECIATION

Ecological speciation: speciation driven by divergent selection

“magic trait”: divergent selection + assortative mating

post-zygotic reproductive

isolation pre-zygotic reproductive

isolation

Servedio et al. 2011, TREE

(50)

x

Merril et al. 2012, Proc R Soc B

MIMICRY AS A DRIVER OF SPECIATION

H. melpomene H. cydno

Predation experiments

% attacked

(51)

→ Selection against hybrids with intermediate phenotype

x

Merril et al. 2012, Proc R Soc B

MIMICRY AS A DRIVER OF SPECIATION

H. melpomene H. cydno

(52)

MIMICRY AS A DRIVER OF SPECIATION

Merril et al. 2011, Evolution morphes sous-espèces

→ Assortative mating for wing pattern

(53)

MIMICRY AS A DRIVER OF SPECIATION

→ cascading effects on speciation (super magic trait!)

• mate preference genetically associated with colour pattern

• mate preference genetically associated with hostplant preference

• mimicry pattern associated with hostplant

• assortative mating for wing pattern enhanced by correlation with

microhabitat preference

Merrill et al. 2013, JEB Merrill et al. 2011, PRSB

Elias et al. 2008, PLoS Biol

Willmott and Mallet 2004, Biol Let

(54)

MIMICRY AS A DRIVER OF SPECIATION

• phylogenetic signature

Elias et al. 2007, J Ins Sci

(55)

H. cydno H. heurippa H. melpomene

• H. heurippa genetically and phenotypically intermediate

• artificial generation of hybrid resembling H. heurippa

Mavarez et al. 2006, Nature

HYBRID SPECIATION

(56)

• pre and post- zygotic reproductive isolation

Relative probability of approach

Salazar et al. 2005, JEB Mavarez et al. 2006, Nature

HYBRID SPECIATION

(57)

HOW TO BECOME A GOOD MIMIC?

The genetic bases of colour pattern variation

(58)

HOW TO BECOME A GOOD MIMIC?

● Mapping the genetic bases of colour pattern variation

Joron et al. 2006, Heredity Joron et al. 2006, PLoS Biol Huber et al. 2015, Heredity

(59)

HOW TO BECOME A GOOD MIMIC?

H. melpomene

H. erato

Yb Ac Sb N

B D

K

● The mimicry ‘toolkit’ in Heliconius

P

Cr D Sd

Joron et al. 2006, PLoS Biol; Huber et al. 2015 Heredity

(60)

HOW TO BECOME A GOOD MIMIC?

● mimicry genes

Yb Ac Sb N

B D

K

Optix (transcription factor) WntA (signaling ligand)

Reed et al 2011, Science

Martin et al 2011, PNAS

Cortex (cell-cycle regulator)

Nadeau et al 2016, Nature

(61)

Biston betularia ‘carbonaria’ locus Heliconius melpomene yellow loci

Heliconius numata supergene annotation

BigEye Bicyclus anynana BigEye mutant

mapping interval

Saenko et al. 2010 BMC Biol

Van’t hof et al. 2011 Science, 2016 Nature Ferguson et al. 2011 Mol Ecol

Baxter et al. 2011 PLoS Genet Joron et al. 2011, Nature

HOW TO BECOME A GOOD MIMIC?

● mimicry genes

Yb Ac Sb N

B D

K

(62)

● Adaptive introgression in Heliconius

H. melpomene

H. elevatus

H. numata H. timareta

B D vs

LG18 H. cydno

Heliconius Genome consortium 2012, Nature

~ 1 mya

HOW TO BECOME A GOOD MIMIC?

(63)

B

D _LG18

Heliconius Genome consortium 2012, Nature H. melpomene

H. elevatus

H. timareta H. cydno

( )

=

HOW TO BECOME A GOOD MIMIC?

(64)

B

D _LG18

Heliconius Genome consortium 2012, Nature H. melpomene

H. elevatus

H. timareta H. cydno

( )

≠

HOW TO BECOME A GOOD MIMIC?

(65)

EXTENSIVE GENE FLOW

(66)

EXTENSIVE GENE FLOW

(67)

EXTENSIVE GENE FLOW

(68)

EXTENSIVE GENE FLOW

(69)

THE FABULOUS STORY OF

HELICONIUS NUMATA

(70)

THE FABULOUS STORY OF HELICONIUS NUMATA

different

H. numata morphs different

Ithomiini species

(71)

● polymorphic within population

→ How to avoid producing intermediate, non-mimetic phenotypes?

x x

Yb Ac Sb N

B D

K P

→ a single locus determines phenotypic variation

=> supergene ~ 450 kb

? x

Joron et al. 2006, PLoS Biol; 2011 Nature

(72)

● A supergene locked with inversions!

1 2

3 4 5 6

7 8

1

2 4

6

7 8

1

2

3 3

4 5

5

6 7

8 18 genes

13 genes

Joron et al. 2011 Nature

LePoul et al. 2014 Nature Comm

Ancestral Inversion 1 Inversions 1+(2+3)

Recombination impaired

Recombination allowed

● Dominance!

(73)

● Dominance depends on co-occurrence

Phenotype of homozygotes

Phenotype of heterozygotes

X

=

SYMPATRYPARAPATRY =

X

=

Dominance heatmap

→ full dominance

→ mosaic of dominance with colour hierarchy

LePoul et al. 2014 Nature Comm

(74)

local polymorphism

THE FABULOUS STORY OF HELICONIUS NUMATA

Supergene (single locus)

No recombination (inversions)

Dominance in sympatry

Disassortative mating?

P

1 2

3 4 5 6

7 8

1

2 4

6

7 8

1

2

3 3

4 5

5

6 7

8

(75)

MIMICRY AND THE EVOLUTION

OF THE ECOLOGICAL NICHE

(76)

habitat butterfly predator microhabitat niche partitioning

MIMICRY AND THE EVOLUTION

OF THE ECOLOGICAL NICHE

(77)

MIMICRY AND THE EVOLUTION

OF THE ECOLOGICAL NICHE

(78)

Gompert et al. 2011 JTB

→ heterogeneous predation drives

adaptive microhabitat niche convergence

MIMICRY AND THE EVOLUTION

OF THE ECOLOGICAL NICHE

(79)

eurimedia (33%)

hermias (32%)

lerida (10%)

aureliana (8%)

agnosia (7%)

mamercus (5%)

confusa (3%)

mothone (2%) Forbestra equicola

0.1

Oleria gunilla Oleria sexmaculata Oleria assimillis Oleria agarista Oleria onega Oleria ilerdina Hyposcada illinissa Hyposcada anchiala (Hyposcada kena) (Dircenna dero ) Ceratinia tutia Episcada sulphurea (Pteronymia sao) Pteronymia vestilla Pteronymia primula (Callithomia alexirrhoe) Callithomia lenea Godyris zavaleta Heterosais nephele Hypoleria lavinia Brevioleria arzalia Brevioleria seba Pseudoscada timna Pseudoscada florula Hypothyris moebiusi Hypothyris fluonia Hypothyris semifulva Hypothyris anastasia Hypothyris euclea Hypothyris mamercus (Napeogenes quadrilis) Napeogenes aethra Napeogenes pharo Napeogenes achaea Napeogenes duessa Napeogenes sylphis Napeogenes inachia Ithomia salapia Ithomia amarilla Ithomia agnosia Aeria eurimedia Tithorea harmonia Thyridia psidii Scada zibia Mechanitis mazaeus Mechanitis polymnia Mechanitis lysimnia Mechanitis messenoides Mechanitis messenoides Forbestra olivencia (Forbestra proceris) Methona curvifascia Methona confusa Methona grandior Melinaea satevis Melinaea menophilus Melinaea marsaeus Melinaea marsaeus Hyalyris spnov

Elias et al. 2008 PLoS Biol

Are co-mimics ecologically more similar than expected given the phylogeny?

Observed value

→ simulations of microhabitat niche evolution

ecological distances

among co-mimics (simulations)

p < 0.001

(80)

Elias et al. 2008 PLoS Biol

→ adaptive microhabitat niche convergence

MIMICRY AND THE EVOLUTION

OF THE ECOLOGICAL NICHE

(81)

MIMICRY, HABITAT AND HOSTPLANT

(82)

If hostplants highly segregated by microhabitat

→ co-mimics expected to share hostplants more often than at random

MIMICRY, HABITAT AND HOSTPLANT

(83)

Willmott & Mallet 2004 Biol Let

hostplant sharing in 2 out of 5 communities

MIMICRY, HABITAT AND HOSTPLANT

(84)

If hostplants not segregated by microhabitat

→ co-mimics expected to share hostplants less often than at random

MIMICRY, HABITAT AND HOSTPLANT

(85)

• 4 community-level networks ~ 30 Ithomiini species/site

~ 30 hostplant species/site

_Napo

Arco Iris La Bonita

Los Amigos

Elias et al. in prep.

Solanaceae

MIMICRY, HABITAT AND HOSTPLANT

(86)

(87)

(88)

I am your father!

???

(89)

• Do co-mimics share more (or less) plants than expected?

Napo

Arco Iris La Bonita

Los Amigos

vs

MIMICRY, HABITAT AND HOSTPLANT

(90)

Napo

Arco Iris La Bonita

Los Amigos

more

NS

• Do co-mimics share more (or less) plants than expected?

more

MIMICRY, HABITAT AND HOSTPLANT

(91)

• Do co-mimics share more (or less) plants than expected given the

phylogeny?

_Napo

Arco Iris La Bonita

Los Amigos

more

NS

NS NS

MIMICRY, HABITAT AND HOSTPLANT

(92)

Napo

Arco Iris La Bonita

Los Amigos

more

NS

NS NS

more less less NS NS NS NS

MIMICRY, HABITAT AND HOSTPLANT

(93)

MIMICRY, HABITAT AND HOSTPLANT

● community-level patterns often neutral-like

● species in some mimicry rings share more plants than expected

● species in other mimicry rings share less plants than expected

→ mutualistic mimicry drives hostplant shifts cascading effects on speciation

(94)

APOSEMATISM AND TRANSPARENCY

(95)

(96)

TRANSPARENT NON TRANSPARENT

(97)

APOSEMATISM AND TRANSPARENCY

Are transparent species less detectable?

Modelling detectability by predators (Vorobyev & Osorio 1998)

(98)

APOSEMATISM AND TRANSPARENCY

Are transparent species less detectable?

Are transparent species less toxic?

Taste-rejection experiments

(99)

APOSEMATISM AND TRANSPARENCY

0 2 4 6 8 10 12 14

10 12 14 16 18 20 22

detectability

palatability

(100)

CONCLUSION

● Müllerian mimicry: a compelling example of the power of selection

P ₁

2

3 4 5 6

7 8

1

2 4

6

7 8

1

2

3 3

4 5

5

6 7

8

● Müllerian mimicry = positive interactions

communities as tightly knit coevolved assemblages → implications for community responses

to global changes?

→ a good system to study adaptation

(101)

CONCLUSION

● Origin of mimicry Ultimate causes:

Fritz Müller, 1879

Proximate causes: parallel evolution, introgression, convergence?

H. melpomene

H. erato

Yb Ac Sb N

B D

K

Cr D Sd

(102)

PERSPECTIVES

● Origin of polymorphism?

- Why do novel phenotypes seem to appear so readily?

- How can novel phenotypes become established?

- Is H. numata a Batesian mimic?

(103)

Credits

Mathieu Joron, CEFE Montpellier Violaine Llaurens, MNHN Paris Chris Jiggins, U Cambridge

Kanchon Dasmahapatra, U York Jim Mallet, U Harvard

Bob Reed, U Cornell Zach Gompert, U Utah

Keith Willmott, U Gainesville