convergent fruit evolution in athysanus and thysanocarpus (brassicaceae) p.j. alexander (1), i.a....
TRANSCRIPT
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.
Consensus of 149 most parsimonious trees.WinClada settings:hold= 25001mult= 2500hold/= 10
Support estimated from 100 bootstrap replicates with 100 mults each.
Streptanthella longirostris
Thysanocarpus conchuliferus
Thysanocarpus laciniatus
Thysanocarpus laciniatus var. crenatus
Thysanocarpus laciniatus var. laciniatus 1
Thysanocarpus laciniatus var. laciniatus 2
Thysanocarpus laciniatus var. laciniatus 3
Thysanocarpus radians 1
Thysanocarpus radians 2
Thysanocarpus radians 3
Thysanocarpus curvipes var. eradiatus 1
Thysanocarpus curvipes var. eradiatus 3
Thysanocarpus curvipes 3
Thysanocarpus curvipes var. eradiatus 2
Thysanocarpus curvipes 1
Thysanocarpus curvipes 5
Thysanocarpus curvipes 4
Thysanocarpus curvipes var. elegans 2
Thysanocarpus curvipes var. elegans 1
Thysanocarpus curvipes var. curvipes
Thysanocarpus curvipes 2
Thysanocarpus curvipes var. elegans 4
Thysanocarpus curvipes var. elegans 3
Thysanocarpus curvipes var. elegans 5
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.
Streptanthella longirostris
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
Athysanus pusillusHeterodraba unilateralis
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
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41
60
20
3
6
5
4523
29
18
98
6868
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1
884
11
9
55
8253
7067
4799
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79
76
5594
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5347
7998
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24
23
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37 Draba species
9 Draba species
8 Draba species
32 Draba species
Arabis
Draba
Draba
§ Erophila
§ Tomostima
Draba
Phylogeny of Arabideae fromITS data.
Consensus of 59694 most parsimonious trees.WinClada settings:hold= 100001mult= 10000hold/= 10
Support estimated from 100 bootstrap replicates with 100 mults each.
9231
Streptanthella longirostris
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
Athysanus pusillusHeterodraba unilateralis
Draba muralis
Arabis blepharophyllaArabis soyeri
Aubrieta deltoideaPseudoturritis turrita
Draba hystrixArabis alpina
9373
10021
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85
79
47
9030
6824
128
4125
6394
87
11
72
9358
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0
3
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7599
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1823
38
58
47
13
622448
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6
14
7014
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8065
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59
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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
Support estimated from 100 bootstrap replicates with 100 mults each.
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
Streptanthella longirostris
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.
Consensus of 100001 most parsimonious trees.WinClada settings:hold= 100001mult= 10000hold/= 10
Support estimated from 100 bootstrap replicates with 100 mults each.
100
89
54
39100
39
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”
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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?