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Convergent fruit evolution in Athysanus and Thysanocarpus (Brassicaceae). P.J. Alexander (1) , I.A. Al-Shehbaz (2) , G. Rajanikanth (1) , C.D. Bailey (1) , and M.D. Windham (3) (1) New Mexico State University; (2) Missouri Botanical Garden; (3) University of Utah. Introduction

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slide1

Convergent fruit evolution in Athysanus and Thysanocarpus

(Brassicaceae)

P.J. Alexander (1) , I.A. Al-Shehbaz (2), G. Rajanikanth (1), C.D. Bailey (1), and M.D. Windham (3)

(1) New Mexico State University; (2) Missouri Botanical Garden; (3) University of Utah

slide2

Introduction

In the mustard genus Athysanus, fruit and trichome morphology give conflicting evidence of generic affinities. Its unusual fruit morphology is shared with Thysanocarpus, which is similar in other respects as well. However, trichome morphology differs between the two genera, and suggests a closer affinity of Athysanus to genera such as Heterodraba,Draba, or Alyssum.

We generated sequence data from ITS and trnL to discover the generic affinities of Athysanus, Heterodraba, and Thysanocarpus and better understand evolution in the group.

slide4

Thysanocarpus:

  • six species, Thysanocarpus curvipes & T. laciniatus widespread
  • white-flowered desert annuals in the SW US & adjacent Mexico
  • fruits with 1 carpel, 1 seed, indehiscent, winged
  • glabrous or with sparse, simple trichomes
slide5

Athysanus:

  • monotypic, Athysanus pusillus
  • small, white-flowered desert annual in western North America from southern British Columbia to Baja California
  • fruits with one carpel, 1 seed, indehiscent
  • pubescent with simple and rayed trichomes
slide6

Heterodraba:

  • monotypic, Heterodraba unilateralis
  • small, white-flowered desert annual in California and S Oregon
  • fruits with 2 carpels, 6-12 seeds, +/- indehiscent
  • pubescent with simple and rayed trichomes
slide7

Athysanus affinities?

  • Thysanocarpus is placed in Schizopetaleae with weak support in ITS trees (Bailey et al., in review; Al-Shehbaz et al., 2006)
  • Athysanus & Heterodraba not previously investigated with genetic data; both placed in Alysseae (Schulz, 1936) or Arabideae (Al-Shehbaz, 2006) based on morphology
  • So: is Athysanus related to Thysanocarpus, as suggested by fruit morphology, or within one of the branched-trichome clades like Alysseae or Arabideae?
slide8

Methods

We generated ITS and trnL sequence data for these three genera and several outgroups;

We downloaded ITS and trnL sequences from GenBank;

We aligned sequences using with ClustalW (Thompson et al., 1994);

We scored gap characters with GapCoder (Simmons et al., 2001; Young & Healy, 2003);

5. We produced maximum parsimony trees with NONA (Goloboff, 2000) via WinClada (Nixon, 1999-2002).

slide9

Aethionema arabicum

Biscutella laevigata

Phylogeny of Brassicaceae from ITSdata.

Consensus of 58 most parsimonious trees.

WinClada settings:

hold= 25001

mult= 2500

hold/= 10

Support estimated from 100 bootstrap replicates with 100 mults each.

9

6

Alyssum alyssoides

Aurinia saxatile

Neotorularia torulosa

4

8

Lobularia maritima

3

6

1

0

0

Noccaea montana

Microthlaspi perfoliatum

3

4

Notothlaspi australe

Sisymbrium loesellii

9

8

Sisymbrium irio

Thellungiella salsuginea

9

2

9

8

Eutrema wasabi

Pseudoturritis turrita

6

4

Scolixon mexicanus

Arabis hirsuta

4

0

6

0

Arabideae

70

Arabis alpina

94

Draba mogollonica

98

Draba tomentosa

2

0

94

Heterodraba unilateralis

Athysanus pusillus

Sinapidendron angustifolium

Eruca pinnatifida

9

8

Zilla macroptera

Brassica nigra

6

8

6

2

Raphanus sativus

Hemicrambe fruticulosa

1

0

0

Matthiola incana

4

8

Hesperis matronalis

2

0

4

0

Heliophila arenaria

7

6

Iberis amara

Chamira circaeoides

Sibara rosulata

Sisymbrium andinum

Fourraea alpina

32

Thelypodiopsis vaseyi

Schizopetaleae

Isatis tinctoria

Stanleya pinnata

7

0

Caulanthus inflatus

8

4

Streptanthus cordatus

82

Thysanocarpus laciniatus

94

Thysanocarpus radians

Thysanocarpus curvipes

Barbarea vulgaris

1

0

0

Cardamine hirsuta

8

2

Nasturtium officinale

1

0

0

Rorippa officinale

Ianhedgea minutiflora

7

8

1

0

0

1

0

0

Descurainia californica

Descurainia pinnata

Smelowskia johnsonii

1

0

0

6

0

Smelowskia americana

7

2

Lepidium oleraceum

1

0

0

Lepidium virginianum

1

0

0

Thlaspi arvense

4

2

Capsella bursa-pastoris

9

2

Camelina microcarpa

Olimarabidopsis pumila

7

2

Physaria fendleri

1

0

0

Nerisyrenia linearifolia

1

0

0

2

8

Lyrocarpa coulteri

Arabidopsis halleri ssp. halleri

1

0

0

Arabidopsis thaliana

2

8

Transberingia bursifolia

Boechera perennans

7

0

4

4

Nevada holmgrenii

6

2

Boechera laevigata

Sphaerocardamum macropetalum

9

8

Mancoa pubens

1

0

0

Halimolobos diffusa

slide10

Streptanthella longirostris

Phylogeny of Thysanocarpus from combined ITSand trnL data.

Consensus of 149 most parsimonious trees.

WinClada settings:

hold= 25001

mult= 2500

hold/= 10

Support estimated from 100 bootstrap replicates with 100 mults each.

Thysanocarpus conchuliferus

Thysanocarpus laciniatus

93

Thysanocarpus laciniatus var. crenatus

93

T. laciniatus

Thysanocarpus laciniatus var. laciniatus 1

Thysanocarpus laciniatus var. laciniatus 2

82

Thysanocarpus laciniatus var. laciniatus 3

Thysanocarpus radians 1

100

T. radians

Thysanocarpus radians 2

Thysanocarpus radians 3

Thysanocarpus curvipes var. eradiatus 1

Thysanocarpus curvipes var. eradiatus 3

89

Thysanocarpus curvipes 3

Thysanocarpus curvipes var. eradiatus 2

Thysanocarpus curvipes 5

Thysanocarpus curvipes 4

96

Thysanocarpus curvipes 1

T. curvipes

Thysanocarpus curvipes var. elegans 2

Thysanocarpus curvipes var. elegans 1

Thysanocarpus curvipes var. curvipes

Thysanocarpus curvipes 2

Thysanocarpus curvipes var. elegans 4

83

Thysanocarpus curvipes var. elegans 3

75

Thysanocarpus curvipes var. elegans 5

slide11

Thysanocarpus in Schizopetaleae...

  • Apart from Thysanocarpus, Schizopetaleae includes exclusively plants with long, narrow, bicarpellate, many-seeded fruits.
  • Most members of the tribe are similar to Thysanocarpus in being glabrous or with only sparse, simple trichomes. The tribe also includes a number of taxa with similar ecology.
slide12

Streptanthella longirostris

Pseudoturritis turrita

Draba

Draba muralis

Draba hystrix

Aubrieta deltoidea

76

70

Draba funiculosa

Arabis alpina

62

Arabis bryoides

98

Arabis procurrens

23

Arabis

79

53

Arabis hirsuta

Phylogeny of Arabideae from

ITSdata.

Consensus of 59694 most parsimonious trees.

WinClada settings:

hold= 100001

mult= 10000

hold/= 10

Support estimated from 100 bootstrap replicates with 100 mults each.

Arabis soyeri

47

Arabis scabra

57

Arabis flagellosa

94

Arabis nuttallii

55

Arabis blepharophylla

24

§ Erophila

100

Draba spathulata

Draba verna

37 Draba species

Draba reptans

Draba

99

§ Tomostima

Draba cuneifolia

47

Draba araboides

Draba platycarpa

79

Draba jaegeri

30

Draba ramosissima

Draba hitchcockii

65

Draba pterosperma

Draba nemorosa

9

92

Heterodraba unilateralis

31

Athysanus pusillus

Draba rigida

70

Draba bruniifolia

67

Draba lasiocarpa

53

Draba cryophila

82

Draba bellardii

Draba aizoides

55

Draba cuatrecasana

Draba elata

4

Draba yunnanensis

88

Draba surculosa

9 Draba species

11

Draba koeiei

98

Draba olgae

Draba radicans

32

Draba aubrietioides

Draba setosa

68

1

Draba cachemirica

68

Draba oreades

Draba asprella

Draba

Draba juniperina

Draba crassifolia

29

Draba densifolia

23

Draba pulvinata

45

18

Draba pycnophylla

Draba brachystylis

8 Draba species

5

Draba sobolifera

63

Draba subalpina

32 Draba species

6

Draba barclayana

41

Draba standleyi

Draba boyacana

Draba confertifolia

3

Draba stylosa

60

Draba violacea

Draba depressa

Draba pickeringii

Draba farsetioides

20

Draba litamo

Draba hallii

slide13

Streptanthella longirostris

Arabis alpina

Draba hystrix

Arabis

Draba

98

100

Arabis blepharophylla

47

Arabis soyeri

39

Aubrieta deltoidea

Pseudoturritis turrita

93

Draba muralis

99

Heterodraba unilateralis

42

Athysanus pusillus

Draba cuneifolia

§s Abdra & Tomostima

Draba reptans

34

Draba platycarpa

Phylogeny of Arabideae from

trnL data.

Consensus of 37225 most parsimonious trees.

WinClada settings:

hold= 100001

mult= 10000

hold/= 10

--final swapping after mult completion was

terminated early

Support estimated from 100 bootstrap replicates with 100 mults each.

Draba araboides

61

Draba brachycarpa

25 Draba species

Draba stylaris

83

Draba carinthiaca

Draba ladina

Draba farsetioides

52

89

Draba fladnizensis

99

Draba aizoides

75

Draba cuatrecasana

Draba pennell hazenii

Draba laurentiana

51

Draba hirta

59

24

Draba arseniewii

Draba lanceolata

Draba lactea

65

Draba alpina

80

Draba winterbottomii

Draba altaica

Draba radicans

59

47

Draba macbeathiana

Draba alberti

85

Draba nemorosa

Draba hispida

79

Draba lasiocarpa

21

100

Draba lutescens

58

Draba huetii

3

Draba jucunda

73

Draba gracillima

93

Draba ellipsoidea

Draba eriopoda

Draba hyperborea

72

Draba aubrietioides

39

Draba stenocarpa

Draba trinervis

58

53

93

Draba olgae

Draba

0

Draba odudiana

§ Erophila

Draba longisiliqua

30

90

Draba verna

11

Draba hederifolia

Draba mollissima

87

Draba heterocoma

94

Draba cuspidata

63

Draba natolica

25

Draba scardica

41

Draba hispanica

8

Draba cretica

12

Draba oreadum

24

68

Draba parnassica

Draba lacaitae

21 Draba species

91

Draba streptocarpa

Draba rositae

Draba incana

51

Draba spectabilis

14

97

Draba jaegeri

70

Draba incerta

Draba magellanica

76

Draba norvegica

Draba kotschyi

14

Draba breweri

Draba aurea

6

Draba gilliesii

Draba tucumanensis

43

Draba paysonii

Draba hitchcockii

Draba glabella

Draba athoa

Draba pusilla

Draba aureola

40 Draba species

99

Draba juniperina

23

18

Draba micropetala

Draba stenopetala

48

Draba wurdackii

62

24

Draba alyssoides

Draba lapaziana

38

Draba obovata

Draba pauciflora

13

58

Draba subalpina

Draba kassii

47

Draba melanopus

Draba bhutanica

slide14

Phylogeny of Arabideae from combined ITS and trnL data.

Streptanthella longirostris

Draba muralis

Draba

Arabis alpina

Draba hystrix

73

Aubrieta deltoidea

78

Pseudoturritis turrita

Arabis bryoides

100

Arabis procurrens

59

47

Arabis soyeri

Arabis hirsuta

41

Arabis

Consensus of 100001 most parsimonious trees.

WinClada settings:

hold= 100001

mult= 10000

hold/= 10

Support estimated from 100 bootstrap replicates with 100 mults each.

Arabis scabra

57

Arabis flagellosa

94

67

Arabis blepharophylla

Arabis nuttallii

Heterodraba unilateralis

100

Athysanus pusillus

Draba hederifolia

73

§ Erophila

Draba verna

89

Draba spathulata

157 Draba species

Draba globosa

39

41

Draba kassii

Draba burkei

54

Draba incana

50

Draba jaegeri

88

Draba incerta

Draba magellanica

Draba bellardii

71

Draba cryophila

48

39

67

Draba aizoides

Draba cuatrecasana

Draba

Draba lutescens

Draba huetii

12

Draba lasiocarpa

Draba rigida

Draba bruniifolia

39

Draba brachycarpa

100

Draba reptans

Draba platycarpa

68

§s Abdra & Tomostima

50

Draba cuneifolia

Draba araboides

Draba mollissima

77

Draba heterocoma

83

Draba cuspidata

58

Draba natolica

18

Draba scardica

32

Draba hispanica

8

Draba cretica

16

Draba oreadum

20

56

Draba parnassica

Draba lacaitae

slide15

Athysanus and Draba

  • Although some Draba have shortened, nearly orbicular fruits, the single-seeded, unicarpellate fruits of Athysanus are unique in Arabideae.
  • In other gross features, Athysanus is quite dissimilar from most Draba; most Draba are alpine to subalpine plants, typically perennial and yellow-flowered.
slide16

Athysanus and Draba

  • The only New World Draba that are white-flowered and annual are in the Abdra/Tomostima clade, which also includes the New World’s only arid and semiarid Draba.
  • Old World white-flowered annual Draba include § Erophila.
  • Our analyses place either § Erophila or §s Abdra & Tomostima basal or sister to the remaining Draba, but resolution is insufficient to allow analysis of evolution of these characters.
slide17

Conclusions

  • Fruit similarities between Athysanus and Thysanocarpus represent convergent evolution. Trichomes better predict relationships in this case.
  • Athysanus is sister to Heterodraba, and the two are either nested within or sister to Draba, depending on the data set used.
  • Thysanocarpus is weakly supported as a member of Schizopetaleae, but does not show a close relationship with any other genera within the tribe.
slide18

The Future: Beyond Phylogeny

  • In addition to Athysanus and Thysanocarpus, Lepidium, Idahoa, Lunaria, Alyssum, Thlaspi, and Noccaea are other prominent genera with reduced fruits, all apparently independently derived,
  • So now we have a pattern that seems to demand explanation!
  • Some possibilities:
    • reduced per-fruit investment allows quicker reproduction and better fine-tuning of fruit production to resource availability
    • fewer seeds/fruit may mean larger seeds, which may provide rapid seedling establishment needed in temporally- limited habitats
    • fewer seeds/fruit may have dispersal advantages by lowering the density of fruits
    • few-seeded fruits with large photosynthetic area may be able to “pay for themselves”
slide19

Cited works:

      • Al-Shehbaz IA, Beilstein MA, Kellogg EA (2006) Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Plant Systematics and Evolution 259, 89-120.
      • Bailey CD, Koch MA, Mayer M, Mummenhoff K, O’Kane SL, Warwick SI, Windham MD, Al-Shehbaz IA (2006) A Global nrDNA ITS Phylogeny of the Brassicaceae. Molecular Biology and Evolution, in review.
      • Bailey CD, Price RA, Doyle JJ (2002) Systematics of the Halimolobine Brassicaceae: Evidence from Three Loci and Morphology. Systematic Botany27, 318-332.
      • Beilstein MA, Al-Shehbaz IA, Kellogg EA (2006) Brassicaceae phylogeny and trichome evolution. American Journal of Botany93, 607-619.
      • de Candolle AP (1821) Cruciferae. Systema Naturale2, 139-700.
      • Goloboff PA (2000) NONA (NO NAME) ver. 2. Published by the author.
      • Koch M, Mummenhoff K (2001) Thlaspi s.str. (Brassicaceae) versus Thlaspi s.l.: morphological and anatomical characters in the light ot ITS nrDNA sequence data. Plant Systematics and Evolution227, 209-225.
      • Nixon KC (1999-2002) WinClada ver. 1.0000. Published by the author.
      • Schulz OE (1936) Cruciferae. In: Die natürlichen Planzenfamilien eds. Engler A, Harms H). Wilhelm Engelmann, Leipzig, Germany.
      • Simmons MP, Ochoterena H, Carr TG (2001) Incorporation, Relative Homoplasy, and Effect of Gap Characters in Sequence-Based Phylogenetic Analyses. Systematic Biology50, 454-462.
      • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673-4680.
      • Young ND, Healy J (2003) GapCoder automates the use of indel characters in phylogenetic analysis. BMC Bioinformatics 4, 6.
  • Acknowledgements:
  • NMSU Dept of Biology and NSF EF-0542228 (CDB)