Paulo Eugênio Oliveira

Universidade Federal de Uberlândia - MG

Reproductive strategies in

Cerrado plants: outcrossing vs.

apomixis and the organization of

plant-pollinator interaction webs

in Central Brazil

Felipe Ribeiro

Cerrado:Neotropical savanna

areas in Central Brazil

Cerrado Physiognomies

Gallery

forestCampos Cerrado Cerradão

Deforestation and

land use in Cerrado

Klink & Moreira 2002

Cerrado as a conservation hot spot

Native areas44,53%

Cultivatedpastureland41,56%

others

0,59%

Urban areas1,90%

Forestry

0,07%

Agriculture

11,35%

Mendonça e at (1998), Ratter et al (2003), Felfili et al (2001), Sano et al. (2008)

376sites

Ratter et al, 2003

Bridgewater et al. 2004

Floristic basis

• Woody species = 953 spp

• Herbs/woody ratio= 3-4/1

• No species occurred in all sites

• Gallery forest and riverine woody species = 1 900 spp

• Total = > 12000 spp

High β diversity and

species turn-over

Cerrado Determinants

Nutrient

poor soils

FireSeasonal

climate

Woody species with

deep roots

Herbaceous plants

with shallow root

system

Water use and

seasonality

Accumulated biomass and fire

Fire

Traditional ideas suggested fire and environmental

restrictions would render sexual reproduction of woody

species very difficult and would favor asexual reproduction

Gallery

forestCampos Cerrado Cerradão

Gallery

forestCampos Cerrado Cerradão

Malvaceae (Gottsberger 1986)

Malvaceae (Gottsberger 1986)

Woody hummingbirds and

bat pollinated species with

specialized flowersHerbaceous

bee pollinated

promiscuous groups

Diversity of pollination systems

Oliveira & Gibbs 2000

Cerrado Dry Secondary Cloudy Dry Lowland

forest forest forest forest rainforest

BSB Costa Rica Venezuela Venezuela Mexico Costa Rica

Dioecy 15 22 24 31 20 23

Monoecy 5 10 0 3 10 11

Self-incompat. 66 54 64 26 53 53

Autogamous 14 14 12 43 17 13

Outcrossing 81 76 88 57 73 75

Breeding systems of woody species in Netropical areas

Oliveira & Gibbs 2000

Polinizadores, vicariancia, fenologia e processo de especiaçãoV. pumila

V. pyramidalis

V. rufa

V. thyrsoidea

V. tucanorum

V. elliptica

Oliveira & Gibbs 1994

Polinizadores, vicariancia, fenologia e processo de especiaçãoV. pumila

V. pyramidalis

V. rufa

V. thyrsoidea

V. tucanorum

V. elliptica

Oliveira & Gibbs 1994

Distribution of Vochysia (Vochysiaceae)

in Cerrado plant formations.

- self-incompatible

- dependent on large bees for fruit set.

- guild of plants (including other groups) and large bees

Sphingids Plants

Guilds and interaction web

Amorim 2008

Average flower lenght (cm)

Av

era

ge

pro

bo

scis

len

gh

t (c

m)

Blind connections: association between

hawkmoths and plants in Cerrado.

Amorim 2008

1,25 cm

1,25 cm1,75cm

1,75cm

Xylocopa (Neoxylocopa) suspecta (Moure & Camargo)

Xylocopa (Neoxylocopa) frontalis (Olivier)

Xylocopa (Neoxylocopa) grisescens Lepeletier

Clá

udia

Inês

da

Silv

a

Cláudia Inês Silva

Pollen load on Xylocopa bees

Xylocopa frontalis

Xylocopa suspecta

Xylocopa grisescens

Xylocopa hirsutissima

30 plant spp. intensely used

Cláudia Inês Silva

Xylocopa frontalis

Xylocopa suspecta

Xylocopa grisecens

Xylocopa hirsutissima

Floral visitors on Matayba

guianensis (Sapindaceae)

in Cerrados of Uberlândia

Ana Coelho Carvalho,

Unpublished data

Wasps

50

Beetles

37

Bees

110

!

Guilds, redundancy and resilience

Obligatory outcrossing: dependency on pollinators.

Specialized relationships are

rare. Generalist guilds?

Redundancy and stability?

Guilds and resilience after

disturbance.

Adjust to high β-diversity?

Importance

of apomixisMelastomataceae

Miconieae39%

63%

Eriotheca pubescens

Goldenberg & Shepherd 1998Oliveira et al. 1992

Martins & Oliveira 2003

Mendes-Rodrigues et al. 2005

Grupos EspecíficosSpecific groups

Polyembryony

and apomixis

Salomão & Allem 2001

Allem 2003

Apomixis in Cerrado

Questions:

How common is polyembryony among cerrado plants?

Is polyembryony a diagnostic feature to estimate

importance of apomixis in Cerrado plants?

How widespread are polyembryony and apomixis in

Cerrado environment?

What is the origin of apomictic taxa?

Consequences and perspectives?

Apomixis in Cerrado plantsCNPq research grant (2005-2007)

Family Species Method Mean SD N SE Min. Max Mono Poly %M %P

Anacardiaceae Astronium fraxinifolium Embryos 1,00 0,00 253,00 0,00 1,00 1,00 253,00 0,00 100,00 0,00

Anacardiaceae Astronium fraxinifolium Seedlings 1,01 0,08 697,00 0,00 1,00 2,00 692,00 5,00 99,28 0,72

Anacardiaceae Lithraeae molleoides Seedlings 1,00 0,00 1.335,00 0,00 1,00 1,00 1.335,00 0,00 100,00 0,00

Anacardiaceae Myracrodruon urundeuva Embryos 1,01 0,11 250,00 0,01 1,00 2,00 247,00 3,00 98,80 1,20

Anacardiaceae Myracrodruon urundeuva Seedlings 1,01 0,10 486,00 0,00 1,00 2,00 481,00 5,00 98,97 1,03

Apocynaceae Aspidosperma cylindrocarpum Seedlings 1,00 0,00 221,00 0,00 1,00 1,00 221,00 0,00 100,00 0,00

Bignoniaceae Jacaranda cuspidifolia Seedlings 1,01 0,11 404,00 0,01 1,00 3,00 402,00 2,00 99,50 0,50

Bignoniaceae Tabebuia avellanedae Seedlings 1,00 0,00 346,00 0,00 1,00 1,00 346,00 0,00 100,00 0,00

Bignoniaceae Tabebuia caraiba Seedlings 1,00 0,00 132,00 0,00 1,00 1,00 132,00 0,00 100,00 0,00

Bignoniaceae Tabebuia chysotricha Embryos 2,18 1,12 606,00 0,05 1,00 7,00 192,00 414,00 31,68 68,32

Bignoniaceae Tabebuia chysotricha Seedlings 1,66 0,74 563,00 0,03 1,00 5,00 270,00 293,00 47,96 52,04

Bignoniaceae Tabebuia ochracea Seedlings 1,36 0,48 45,00 0,07 1,00 2,00 29,00 16,00 64,44 35,56

Bignoniaceae Tabebuia roseo-alba Seedlings 1,01 0,08 676,00 0,00 1,00 2,00 672,00 4,00 99,41 0,59

Bignoniaceae Tabebuia serratifolia Embryos 1,26 0,57 46,00 0,08 1,00 4,00 36,00 10,00 78,26 21,74

Bignoniaceae Tabebuia serratifolia Seedlings 1,18 0,38 200,00 0,03 1,00 2,00 165,00 35,00 82,50 17,50

Caesalpiniaceae Copaifera langsdorfii Seedlings 1,00 0,04 577,00 0,00 1,00 2,00 576,00 1,00 99,83 0,17

Caesalpiniaceae Hymenaea courbaril Seedlings 1,00 0,03 1.173,00 0,00 1,00 2,00 1.172,00 1,00 99,91 0,09

Caesalpiniaceae Senna sylvestris Seedlings 1,00 0,05 346,00 0,00 1,00 2,00 345,00 1,00 99,71 0,29

Clusiaceae Kielmeyera coriaceae Embryos 1,00 0,00 62,00 0,00 1,00 1,00 62,00 0,00 100,00 0,00

Clusiaceae Kielmeyera grandiflora Embryos 1,00 0,00 200,00 0,00 1,00 1,00 200,00 0,00 100,00 0,00

Clusiaceae Kielmeyera variabilis Embryos 1,00 0,00 50,00 0,00 1,00 1,00 50,00 0,00 100,00 0,00

Cocholospermaceae Cocholospermum regium Embryos 1,00 0,00 62,00 0,00 1,00 1,00 62,00 0,00 100,00 0,00

Connaraceae Rourea induta Embryos 1,03 0,16 40,00 0,03 1,00 2,00 39,00 1,00 97,50 2,50

Erythroxylaceae Erythroxylum daphnites Embryos 1,00 0,00 139,00 0,00 1,00 1,00 139,00 0,00 100,00 0,00

Euphorbiaceae Manihot anomala Embryos 1,00 0,00 60,00 0,00 1,00 1,00 60,00 0,00 100,00 0,00

Polyembryony analysis

Seeds from 10 different

plants for each species in

the triângulo mineiro region

Polyembryony and apomixis

Our survey: 70 species – 27 families

Total (+ Salomão & Allem): 125 species – 39 families

Apomictics?

Monoembryonic

Polyembryonic

57%

29%

71%

Monoembryonic

Polyembryonic43%

0,00

10,00

20,00

30,00

40,00

50,00

60,00

70,00

80,00

90,00

0 20 40 60 80 100 120 140

6%

23%71%

5%

Polyembryonic

and apomictic ?

Monoembryonic

Polyembryonic

< 5 % seeds

Polyembryonic

> 5 % seeds

Species ranked by

frequency of

apomictic seeds

Polyembryonic species and breeding systems

Family Species Polyembryony % Source BS

Anacardiaceae Astronium fraxinifolium Poli 0,72 Original data Dioecious

Anacardiaceae Myracrodruon urundeuva Poli 2,00 Original data Dioecious

Anacardiaceae Tapirira guianensis Poli 2,00 Salomão e Allem 2001 Dioecious

Apocynaceae Hancornia speciosa Poli 5,00 Salomão e Allem 2001 SI

Bignoniaceae Jacaranda cuspidifolia Poli 0,50 Original data ni

Bignoniaceae Tabebuia chysotricha Poli 68,32 Original data Apomictic

Bignoniaceae Tabebuia ochracea Poli 35,56 Original data SI/Apomictic

Bignoniaceae Tabebuia roseo-alba Poli 0,59 Original data SI

Bignoniaceae Tabebuia serratifolia Poli 21,74 Original data SI/Apomictic

Burseraceae Commiphora lepthophloeos Poli 2,00 Salomão e Allem 2001 ni

Caesalpiniaceae Copaifera langsdorfii Poli 0,17 Original data SI

Caesalpiniaceae Hymenaea courbaril Poli 0,09 Original data SI

Caesalpiniaceae Senna sylvestris Poli 0,29 Original data SI

Connaraceae Rourea induta Poli 2,50 Original data SI

Fabaceae Machaerium acutifolium Poli 2,22 Original data ni

Fabaceae Ormosia arborea Poli 0,25 Original data ni

Flaucortiaceae Casearia sylvestris Poli 0,89 Original data SC

Hippocrateaceae Salacia campestris Poli 2,08 Original data ni

Hippocrateaceae Salacia crassifolia Poli 1,94 Original data ni

Malpighiaceae Byrsonima basiloba Poli 3,00 Salomão e Allem 2001 ni

Malvaceae Eriotheca pubescens Poli 81,82 Original data Apomictic

Malvaceae Guazuma ulmifolia Poli 1,21 Original data SI

Melastomataceae Clidemia hirta Poli 12,53 Original data Apomictic

Melastomataceae Miconia albicans Poli 1,51 Original data Apomictic

Melastomataceae Miconia ferruginata Poli 24,74 Original data Apomictic

Mimosaceae Acacia polyphylla Poli 2,00 Original data

Mimosaceae Inga laurina Poli 41,33 Original data Apomictic?

Myrtaceae Campomanesia pubescens Poli 0,12 Original data SI/SC

Myrtaceae Eugenia calycina Poli 1,31 Original data ni

Myrtaceae Eugenia hegeliana Poli 3,40 Original data ni

Myrtaceae Eugenia punicifolia Poli 0,45 Original data SC

Rhamnaceae Zizyphus joazeiro Poli 2,00 Salomão e Allem 2001 SC

Rubiaceae Genipa americana Poli 3,00 Salomão e Allem 2001 Dioecious

Sapindaceae Magonia pubescens Poli 3,00 Salomão e Allem 2001 ni

Vochysiaceae Callisthene fasciculata Poli 0,22 Original data SI

Vochysiaceae Callisthene major Poli 0,57 Original data SI

36 species

17 families

At least 11 SI

Contrasting

breeding

system results

in some

putative

apomictics

Polyembryony

without apomixis

Callisthene species

(Vochysiaceae)

R. Carmo-Oliveira & L.N. Custódio

unpublished data

Callisthene fasciculata

Callisthene major

Callisthene major

Callisthene fasciculata

Qualea multiflora

Eriotheca pubescensMendes-Rodrigues et al. 2005 Plant biology 7:533-540

Polyembryony and

sporophitic apomixis

Eriotheca pubescensEriotheca gracilipes

Embryos and seedlings per seed of Tabebuia chrysotricha (embryos n =

606 seeds; seedlings n = 640 seeds).

0

5

10

15

20

25

30

35

40

45

1 2 3 4 5 6 7

Number

Fre

qu

ency

(%

)

Embryos

Seedlings

Costa et al. 2004

Sampaio et al. 2007

Handroanthus (syn. Tabebuia)

Bignoniaceae

Apomixis and Neopolyploidy

Oliveira et al. 1992 Sampaio et al. 2008

2n= 276

2n = 40

2n = 80

Eriotheca pubescens

Miconia albicans

Caetano 2007

Apomixis without polyembryony

Goldenberg & Shepherd 1998 Cortez et al. 2008

How widespread are

apomictic taxa?

Handroanthus ochraceus

Eriotheca pubescens

Miconia albicans

Between the 125 most

frequent woody species in

Cerrado (ca. 1000 spp.)

Bridgewaters et al. 2004

2n=40

2n=80

Polyembryonic

individuals

A

100 Km

BA

100 Km

B

Monoembryonic

individuals

Handroanthus ochraceus

(syn. Tabebuia ochracea)

Eriotheca pubescens

Breeding systems mosaics?

Mila et al. in preparation

Breeding system and

distribution in the

Melastomataceae

40%75%

84%

60%

25%16%

0

5

10

15

20

25

30

35

40

Apomictis Self-incompatible Self compatible

Breeding system

Sp

ec

ies

wide

restrict

Apomictics widespread

Questions:

How common is polyembryony among cerrado plants?

Is polyembryony a diagnostic feature to estimate

importance of apomixis in Cerrado plants?

How widespread are polyembryony and apomixis in

Cerrado environment?

What is the origin of apomictic taxa?

±Hybridization?

Polyploidy?

Widely distributed apomictics

Consequences: apomixis as a reproductive alternative ?

Foto: Rogério Gribel

Collevatti, R.G., Grattapaglia, D., & Hay, J.D. 2001. Population genetic structure of the endangered

tropical tree species Caryocar brasiliense, based on variability at microsatellite loci. Molecular

ecology 10: 349-356

Collevatti, R.G., Grattapaglia, D., & Hay, J.D. 2001. High resolution microsatellite based analysis of

the mating system allows the detection of significant biparental inbreeding in Caryocar brasiliense,

an endangered tropical tree species. Heredity 86 (1): 60-67

Disturbance and reduced

gene flow

Caryocar brasiliense

Miconia albicans

- Independent of pollinators

- Bird dispersed fruits and viable seeds

- But no pollen for bees

The future of Cerrado ?

Clesnan Mendes-Rodrigues

Diana Sampaio

Ana Paula Mila

Daniela Simão

Renata Carmo-Oliveira

Luciana N. Custódio

Rosana Romero

Pietro K. Maruyama

Felipe W. Amorim

Ana Paula Caetano

Peter E. Gibbs