convergent fruit evolution in athysanus and thysanocarpus (brassicaceae) p.j. alexander (1), i.a....

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

IntroductionIn 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.

Fruits & trichomes

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

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

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

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?

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).

Eruca pinnatifida

68

98

48

76

40

100

62

98

92

96

8470

10036

6040

64

10082

100

100100

100

100100

72

92

100100

100

6270

10098

44

28

28

72

42

60

78

20

20

98

34

48

Zilla macroptera

Athysanus pusillusHeterodraba unilateralis

Draba mogollonicaDraba tomentosa

Arabis alpina

Scolixon mexicanusArabis hirsuta

Pseudoturritis turritaEutrema wasabi

Sisymbrium loeselliiSisymbrium irio

Aethionema arabicum

Aurinia saxatileAlyssum alyssoides

Lobularia maritimaNoccaea montana

Brassica nigraRaphanus sativus

Capsella bursa-pastorisThlaspi arvenseLepidium virginianum

Lepidium oleraceumSmelowskia americana

Physaria fendleriNerisyrenia linearifoliaLyrocarpa coulteri

Arabidopsis thaliana

Nevada holmgreniiBoechera laevigata

Boechera perennans

Mancoa pubensHalimolobos diffusa

Sphaerocardamum macropetalum

Descurainia californicaDescurainia pinnata

Barbarea vulgarisCardamine hirsuta

Streptanthus cordatusCaulanthus inflatus

Stanleya pinnata

Rorippa officinaleNasturtium officinale

Ianhedgea minutiflora

Smelowskia johnsonii

Camelina microcarpaOlimarabidopsis pumila

Arabidopsis halleri ssp. halleri

Transberingia bursifolia

Neotorularia torulosa

Microthlaspi perfoliatumNotothlaspi australe

Thellungiella salsuginea

Sinapidendron angustifolium

Hemicrambe fruticulosaMatthiola incanaHesperis matronalisHeliophila arenariaIberis amaraChamira circaeoides

Sibara rosulata Sisymbrium andinumFourraea alpinaThelypodiopsis vaseyiIsatis tinctoria

Biscutella laevigata

Thysanocarpus laciniatusThysanocarpus radians

Schizopetaleae

Arabideae

Phylogeny of Brassicaceae from ITS data.

Consensus of 58 most parsimonious trees.WinClada settings:hold= 25001mult= 2500hold/= 10

Support estimated from 100 bootstrap replicates with 100 mults each.

Thysanocarpus curvipes

94

9498

70

8294

32

Phylogeny of Thysanocarpus from combined ITS and trnL data.



Streptanthella longirostris

Thysanocarpus conchuliferus

Thysanocarpus laciniatus

Thysanocarpus laciniatus var. crenatus

Thysanocarpus laciniatus var. laciniatus 1



Thysanocarpus radians 1



Thysanocarpus curvipes var. eradiatus 1


Thysanocarpus curvipes 3





Thysanocarpus curvipes var. elegans 2


Thysanocarpus curvipes var. curvipes





96

100

82

93

93

89

83

75

T. laciniatus

T. radians

T. curvipes

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.


Draba pickeringiiDraba farsetioidesDraba litamoDraba hallii

Draba confertifoliaDraba stylosaDraba violaceaDraba depressa

Draba barclayanaDraba standleyiDraba boyacana

Draba pulvinata

Draba cachemiricaDraba setosa

Draba oreades

Draba radicans

Draba yunnanensisDraba surculosa

Draba aubrietioides

Draba elata

Draba koeieiDraba olgae

Draba asprella

Draba pycnophylla

Draba densifolia

Draba juniperinaDraba crassifolia

Draba brachystylis

Draba soboliferaDraba subalpina

Draba hitchcockiiDraba pterosperma

Draba jaegeriDraba ramosissima

Draba cuneifoliaDraba araboidesDraba platycarpa

Draba reptans


Draba nemorosa

Draba aizoidesDraba cuatrecasana

Draba cryophilaDraba bellardii

Draba lasiocarpa

Draba rigidaDraba bruniifolia

Draba spathulataDraba verna

Arabis alpina

Arabis nuttalliiArabis blepharophylla

Arabis flagellosaArabis scabra

Arabis hirsutaArabis soyeri

Arabis procurrensArabis bryoides

Draba muralisDraba hystrix

Aubrieta deltoideaDraba funiculosa

Pseudoturritis turrita

63

41

60

20

3

6

5

4523

29

18

98

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32

1

884

11

9

55

8253

7067

4799

65

30

100

79

76

5594

57

5347

7998

62

24

23

70

37 Draba species

9 Draba species

8 Draba species

32 Draba species

Arabis

Draba

Draba

§ Erophila

§ Tomostima

Draba

Phylogeny of Arabideae fromITS data.



9231


Draba juniperinaDraba micropetalaDraba stenopetala

Draba obovata

Draba subalpinaDraba kassiiDraba melanopusDraba bhutanica

Draba athoaDraba pusillaDraba aureola

Draba wurdackiiDraba alyssoidesDraba lapaziana

Draba pauciflora

Draba macbeathianaDraba alberti

Draba radicans

Draba aubrietioidesDraba stenocarpa

Draba olgaeDraba odudiana

Draba trinervis

Draba vernaDraba hederifolia

Draba laurentiana

Draba winterbottomiiDraba altaica

Draba hirtaDraba arseniewii

Draba lanceolataDraba lacteaDraba alpina

Draba lutescensDraba huetii

Draba gracillimaDraba ellipsoideaDraba eriopoda

Draba jucunda

Draba lasiocarpa

Draba nemorosaDraba hispida

Draba longisiliqua

Draba cuspidataDraba natolica

Draba hispanicaDraba cretica

Draba scardica

Draba oreadumDraba parnassicaDraba lacaitae

Draba heterocomaDraba mollissima

Draba spectabilisDraba incana

Draba jaegeriDraba incertaDraba magellanica

Draba breweri

Draba tucumanensisDraba paysoniiDraba hitchcockiiDraba glabella

Draba norvegicaDraba kotschyi

Draba aureaDraba gilliesii

Draba streptocarpaDraba rositae

Draba fladnizensisDraba aizoidesDraba cuatrecasanaDraba pennell hazenii

Draba farsetioides

Draba stylarisDraba carinthiaca

Draba hyperborea

Draba ladina

Draba brachycarpa

Draba platycarpa

Draba cuneifoliaDraba reptans

Draba araboides


Draba muralis

Arabis blepharophyllaArabis soyeri

Aubrieta deltoideaPseudoturritis turrita

Draba hystrixArabis alpina

9373

10021

58

85

79

47

9030

6824

128

4125

6394

87

11

72

9358

39

0

3

89

7599

52

1823

38

58

47

13

622448

99

76

43

6

14

7014

51

91

97

59

8065

24

83

53

59

34

51

100

3947

98

42

40 Draba species

25 Draba species

21 Draba species

Arabis

§s Abdra & Tomostima

§ Erophila Draba

Draba

Phylogeny of Arabideae fromtrnL data.

Consensus of 37225 most parsimonious trees.WinClada settings:hold= 100001mult= 10000hold/= 10--final swapping after mult completion was terminated early


9399

61

Draba kassii

Draba hederifoliaDraba verna

Draba lutescensDraba huetiiDraba lasiocarpa

Draba cuspidataDraba natolica

Draba hispanicaDraba cretica

Draba scardica

Draba oreadumDraba parnassicaDraba lacaitae

Draba heterocomaDraba mollissima

Draba incanaDraba jaegeriDraba incertaDraba magellanica

Draba aizoidesDraba cuatrecasana

Draba cryophila

Draba brachycarpa

Draba platycarpaDraba cuneifolia

Draba reptans

Draba araboides

Athysanus pusillus

Heterodraba unilateralis

Draba muralis

Arabis blepharophylla

Arabis soyeri

Aubrieta deltoideaPseudoturritis turrita

Draba hystrixArabis alpina


Arabis flagellosa

Arabis nuttallii

Draba bellardii

Arabis bryoides

Draba rigida

Arabis hirsuta

Arabis procurrens

Draba bruniifolia

Draba globosa

Draba burkei

Draba spathulata

Arabis scabra

5620

168

3218

5883

77

12

8850

4139

6748

71

5068

73

6794

57

4741

59100

7378

157 Draba species

Arabis

Draba

§ Erophila

§s Abdra & Tomostima

DrabaPhylogeny of Arabideae from combined ITS and trnL data.



100

89

54

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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.

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.

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.

The Future: Beyond PhylogenyIn 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”

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 Botany 27, 318-332.

Beilstein MA, Al-Shehbaz IA, Kellogg EA (2006) Brassicaceae phylogeny and trichome evolution. American Journal of Botany 93, 607-619.

de Candolle AP (1821) Cruciferae. Systema Naturale 2, 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 Evolution 227, 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 Biology 50, 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)

Questions?

convergent fruit evolution in athysanus and thysanocarpus (brassicaceae) p.j. alexander (1), i.a....

Documents

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