Convergent fruit evolution in Athysanus and Thysanocarpus (Brassicaceae) P.J. Alexander (1), I.A. Al-Shehbaz (2), G. Rajanikanth (1), C.D. Bailey (1),

Presentation on theme: "Convergent fruit evolution in Athysanus and Thysanocarpus (Brassicaceae) P.J. Alexander (1), I.A. Al-Shehbaz (2), G. Rajanikanth (1), C.D. Bailey (1),"— Presentation transcript:

1 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

2 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.

3 Fruits & trichomes

4 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

5 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

6 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

7 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?

8 Methods 1.We generated ITS and trnL sequence data for these three genera and several outgroups; 2.We downloaded ITS and trnL sequences from GenBank; 3.We aligned sequences using with ClustalW (Thompson et al., 1994); 4.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).

9 Eruca pinnatifida 68 98 48 76 40 100 62 98 92 96 84 70 100 36 6040 64 100 82 100 100 100 100 100 100 72 92 100 100 100 62 70 100 98 44 28 28 72 42 60 78 20 20 98 34 48 Zilla macroptera Athysanus pusillus Heterodraba unilateralis Draba mogollonica Draba tomentosa Arabis alpina Scolixon mexicanus Arabis hirsuta Pseudoturritis turrita Eutrema wasabi Sisymbrium loesellii Sisymbrium irio Aethionema arabicum Aurinia saxatile Alyssum alyssoides Lobularia maritima Noccaea montana Brassica nigra Raphanus sativus Capsella bursa-pastoris Thlaspi arvense Lepidium virginianum Lepidium oleraceum Smelowskia americana Physaria fendleri Nerisyrenia linearifolia Lyrocarpa coulteri Arabidopsis thaliana Nevada holmgrenii Boechera laevigata Boechera perennans Mancoa pubens Halimolobos diffusa Sphaerocardamum macropetalum Descurainia californica Descurainia pinnata Barbarea vulgaris Cardamine hirsuta Streptanthus cordatus Caulanthus inflatus Stanleya pinnata Rorippa officinale Nasturtium officinale Ianhedgea minutiflora Smelowskia johnsonii Camelina microcarpa Olimarabidopsis pumila Arabidopsis halleri ssp. halleri Transberingia bursifolia Neotorularia torulosa Microthlaspi perfoliatum Notothlaspi australe Thellungiella salsuginea Sinapidendron angustifolium Hemicrambe fruticulosa Matthiola incana Hesperis matronalis Heliophila arenaria Iberis amara Chamira circaeoides Sibara rosulata Sisymbrium andinum Fourraea alpina Thelypodiopsis vaseyi Isatis tinctoria Biscutella laevigata Thysanocarpus laciniatus Thysanocarpus radians Schizopetaleae Arabideae Phylogeny of Brassicaceae from ITS data. Consensus of 58 most parsimonious trees. WinClada settings: hold= 25001 mult= 2500 hold/= 10 Support estimated from 100 bootstrap replicates with 100 mults each. Thysanocarpus curvipes 94 98 70 82 94 32

10 Phylogeny of Thysanocarpus from combined ITS and 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. 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 89 83 75 T. laciniatus T. radians T. curvipes

11 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.

12 Streptanthella longirostris Draba pickeringii Draba farsetioides Draba litamo Draba hallii Draba confertifolia Draba stylosa Draba violacea Draba depressa Draba barclayana Draba standleyi Draba boyacana Draba pulvinata Draba cachemirica Draba setosa Draba oreades Draba radicans Draba yunnanensis Draba surculosa Draba aubrietioides Draba elata Draba koeiei Draba olgae Draba asprella Draba pycnophylla Draba densifolia Draba juniperina Draba crassifolia Draba brachystylis Draba sobolifera Draba subalpina Draba hitchcockii Draba pterosperma Draba jaegeri Draba ramosissima Draba cuneifolia Draba araboides Draba platycarpa Draba reptans Athysanus pusillus Heterodraba unilateralis Draba nemorosa Draba aizoides Draba cuatrecasana Draba cryophila Draba bellardii Draba lasiocarpa Draba rigida Draba bruniifolia Draba spathulata Draba verna Arabis alpina Arabis nuttallii Arabis blepharophylla Arabis flagellosa Arabis scabra Arabis hirsuta Arabis soyeri Arabis procurrens Arabis bryoides Draba muralis Draba hystrix Aubrieta deltoidea Draba funiculosa Pseudoturritis turrita 63 41 60 20 3 6 5 45 23 29 18 98 68 32 1 88 4 11 9 55 82 53 70 67 47 99 65 30 100 79 76 55 94 57 53 47 79 98 62 24 23 70 37 Draba species 9 Draba species 8 Draba species 32 Draba species Arabis Draba § Erophila § Tomostima Draba Phylogeny of Arabideae from ITS data. Consensus of 59694 most parsimonious trees. WinClada settings: hold= 100001 mult= 10000 hold/= 10 Support estimated from 100 bootstrap replicates with 100 mults each. 92 31

13 Streptanthella longirostris Draba juniperina Draba micropetala Draba stenopetala Draba obovata Draba subalpina Draba kassii Draba melanopus Draba bhutanica Draba athoa Draba pusilla Draba aureola Draba wurdackii Draba alyssoides Draba lapaziana Draba pauciflora Draba macbeathiana Draba alberti Draba radicans Draba aubrietioides Draba stenocarpa Draba olgae Draba odudiana Draba trinervis Draba verna Draba hederifolia Draba laurentiana Draba winterbottomii Draba altaica Draba hirta Draba arseniewii Draba lanceolata Draba lactea Draba alpina Draba lutescens Draba huetii Draba gracillima Draba ellipsoidea Draba eriopoda Draba jucunda Draba lasiocarpa Draba nemorosa Draba hispida Draba longisiliqua Draba cuspidata Draba natolica Draba hispanica Draba cretica Draba scardica Draba oreadum Draba parnassica Draba lacaitae Draba heterocoma Draba mollissima Draba spectabilis Draba incana Draba jaegeri Draba incerta Draba magellanica Draba breweri Draba tucumanensis Draba paysonii Draba hitchcockii Draba glabella Draba norvegica Draba kotschyi Draba aurea Draba gilliesii Draba streptocarpa Draba rositae Draba fladnizensis Draba aizoides Draba cuatrecasana Draba pennell hazenii Draba farsetioides Draba stylaris Draba carinthiaca Draba hyperborea Draba ladina Draba brachycarpa Draba platycarpa Draba cuneifolia Draba reptans Draba araboides Athysanus pusillus Heterodraba unilateralis Draba muralis Arabis blepharophylla Arabis soyeri Aubrieta deltoidea Pseudoturritis turrita Draba hystrix Arabis alpina 93 73 100 21 58 85 79 47 90 30 68 24 12 8 41 25 63 94 87 11 72 93 58 39 0 3 89 75 99 52 18 23 38 58 47 13 62 24 48 99 76 43 6 14 70 14 51 91 97 59 80 65 24 83 53 59 34 51 100 39 47 98 42 40 Draba species 25 Draba species 21 Draba species Arabis §s Abdra & Tomostima § Erophila Draba 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. 93 99 61

14 Draba kassii Draba hederifolia Draba verna Draba lutescens Draba huetii Draba lasiocarpa Draba cuspidata Draba natolica Draba hispanica Draba cretica Draba scardica Draba oreadum Draba parnassica Draba lacaitae Draba heterocoma Draba mollissima Draba incana Draba jaegeri Draba incerta Draba magellanica Draba aizoides Draba cuatrecasana Draba cryophila Draba brachycarpa Draba platycarpa Draba cuneifolia Draba reptans Draba araboides Athysanus pusillus Heterodraba unilateralis Draba muralis Arabis blepharophylla Arabis soyeri Aubrieta deltoidea Pseudoturritis turrita Draba hystrix Arabis 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 56 20 16 8 32 18 58 83 77 12 88 50 41 39 67 48 71 50 68 73 67 94 57 47 41 59 100 73 78 157 Draba species Arabis Draba § Erophila §s Abdra & Tomostima Draba Phylogeny of Arabideae from combined ITS and trnL data. Consensus of 100001 most parsimonious trees. WinClada settings: hold= 100001 mult= 10000 hold/= 10 Support estimated from 100 bootstrap replicates with 100 mults each. 100 89 54 39 100 39

15 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.

16 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.

17 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.

18 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”

19 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)

20 Questions?