Perspectives - The first steps of plant mating system evolution

Plant mating systems have already been the focus of research for over two centuries since the work of Sprengel (1793), who described flower structure and function, and later on Darwin (1876), who investigated the attributes of flower organs and its consequences to species adaptation. After several years of study on plant mating system, much information has been gathered today. Moreover, recurrent studies try to compile and summarize this data in order to improve knowledge on plant reproduction and to advance the research field (Charlesworth and Charlesworth, 1987; Barrett, 2002; Charlesworth and Willis, 2009; Eckert et al., 2010).

The research on plant mating systems, particularly in ecology and evolution, however, is not entirely done. Future studies are still needed to describe it much more in detail and with innovative perspectives. It would be meaningful to improve research on populations under natural conditions, testing the effect of environmental predictors and biotic interactions on reproductive traits. For example, the use of choice experiments could be useful to test the role of pollinators, parasites and florivores on selection of specific flower morphs (i.e.

controlling for size, shape, nectar, etc.), and this could help us understand how floral traits may be selected in the wild. The use of more species in addition to the well-known models could also be used to prove the generality of patterns found at the current studied species with association to phylogeny.

My study also reveals that the use of video recordings on pollinator assessments may represent a substantial improvement on the field of pollination ecology. Traditionally, pollinator visitation has been estimated by relatively short sampling times, such as a couple of hours per focal plant, and with the use of personal observations (e.g. Eckhart, 1991; Conner and Rush, 1996; Engel and Irwin, 2003). On the contrary, time-lapse or video recordings, combined with the use of new available software to manipulate and process image data (e.g.

ClickPoints software, Gerum et al., 2016; camtrapR software, Niedballa et al., 2016; and see Steen, 2016), can open the possibility of analyzing comparatively larger amounts data, especially if the process of video analysis could be coupled with automatic object recognition and counting. Moreover, image data can be more easily retrieved and re-analyzed than personal pollinator observations recorded on paper. Future ecological studies would thus profit from more frequent adoption of automated methods of pollinator visitation recording.

My results also highlight that the spatial component of biotic interactions can bring valuable information and should not be forgotten in ecological studies. Previous results on inbreeding depression and floral trait variation support this assertion, given that the occurrence

of outcrossing and selfing A. lyrata populations also relate to their geographical distribution.

Therefore, to understand the complex interactions of plant species with their environment, including the interactions with antagonists and mutualists, studies should consider taking into account the effect of space on their measurements. For example, the effect of space could be incorporated into statistical models by adding the coordinates of the experimental units, and it has been readily implemented in some software (R package spaMM, Rousset et al., 2016; R package geoRglm, Christensen and Ribeiro Jr, 2015; R package spGLM, Finley and Banerjee, 2015; OpenBUGS 3.2.3, http://openbugs.net/w/FrontPage). The disadvantage of this approach, however, is that the computational time is substantially longer than simpler statistical models, and relative larger sample sizes are required (Korner-Nievergelt et al., 2015).

Also, theoretical models and computer simulations using the increasing accumulation of genetic data and the capacity of new software and hardware could produce more reliable tools to predict the behavior of selfing and outcrossing populations. Furthermore, provided that climate change and habitat disturbance are already a major problem for humanity (and will probably still be in the future), it would also be relevant to investigate the importance of anthropogenic effects on plant reproduction and maintenance in ecosystems. Finally, studies should cover more tropical and sub-tropical species, which are depressingly underrepresented or biased in literature (Clark, 1985; World Conservation Monitoring Centre, 1992). Ideally, the solution for fixing this bias would be to encourage international cooperation between multiple research groups, and to improve the education and research quality on historically marginalized world regions. Science should flourish through the lens of social-economic equality. Now, all of the aforementioned suggestions and initiatives seem a daunting task, of course. Should this task be a reality, however, it would be extremely helpful, fostering healthy progress in the study plant mating system ecology and evolution, and in science in general.

Part IV

Conclusions

First, I showed how levels of inbreeding depression may be expressed over different lifecycle stages in outcrossing and selfing populations. Inbreeding depression depends on the trait of study. The evolution of selfing from self-incompatibility not necessarily requires the purging of the genetic load, if inbreeding depression is already low in the species. Moreover, environmental stress does not necessarily produce an increase in the magnitude of inbreeding depression.

Second, I showed how the evolution of selfing in relatively recent selfing lineages may lead to subtle changes in floral morphology. The evolution of mating systems might produce significant changes in flower morphology with varying intensities, depending on the trait of study, but also on the species’ genetic population structure. Thus, evolutionary histories might have important implications to selection of floral traits inside each lineage.

Third, I could not prove that floral trait variation in outcrossing and selfing populations explain pollinator visitation in a common-garden experiment. After the early evolution of selfing, selfing species might still similarly attract pollinators to their flowers compared to their outcrossing ancestors. The reasons for the low outcrossing rates in selfing populations in the wild might thus not always be explained by floral trait variation.

Fourth, I showed how ecological interactions might positively or negatively affect floral trait evolution. Mutualistic and antagonistic partners might influence flower morphology evolution by selecting particular traits, which are associated with their foraging behavior.

The output of floral trait selection should be the net-balance result between mutualistic and antagonistic ecological interactions in plants, because they can influence plant performance.

Finally, I hope to have contributed to the progress of research in plant ecology and evolution. Moreover, I hope that the ideas presented at the end of my discussion will also inspire new people to join the field, and new research to be produced.

Part V

References

Ågren, J., and D. W. Schemske. 1993. Outcrossing rate and inbreeding depression in two annual monoecious herbs,Begonia hirsuta andB. semiovata. Evolution47:125–135.

Aichele, D., and M. Golte-Bechtle. 1979. Was blüht denn da?: wildwachsenden Blütenpflanzen Mitteleuropas.

W. Keller & Co., Stuttgart, Germany.

Akino, T., J. Knapp, J. Thomas, and G. Elmes. 1999. Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite ofMyrmica ant colonies. Proceedings of the Royal Society of London B: Biological Sciences 266:1419–1426.

Al-Shehbaz, I. A., and S. L. O’Kane Jr. 2002. Taxonomy and phylogeny ofArabidopsis (Brassicaceae). The Arabidopsis book/American Society of Plant Biologists1:e0001.

Alarcón, M. L., C. Roquet, and J. J. Aldasoro. 2011. Evolution of pollen/ovule ratios and breeding system in Erodium(Geraniaceae). Systematic Botany36:661–676.

Alexandersson, R., and S. D. Johnson. 2002. Pollinator-mediated selection on flower-tube length in a hawkmoth-pollinatedGladiolus (Iridaceae). Proceedings of the Royal Society of London B: Biological Sciences269:631–636.

Als, T. D., D. R. Nash, and J. J. Boomsma. 2002. Geographical variation in host-ant specificity of the parasitic butterflyMaculinea alconin Denmark. Ecological Entomology27:403–414.

Als, T. D., R. Vila, N. P. Kandul, D. R. Nash, S.-H. Yen, Y.-F. Hsu, A. A. Mignault, J. J. Boomsma, and N. E. Pierce. 2004. The evolution of alternative parasitic life histories in large blue butterflies. Nature 432:386–390.

Anderson, I. A., and J. W. Busch. 2006. Relaxed pollinator-mediated selection weakens floral integration in self-compatible taxa ofLeavenworthia (Brassicaceae). American Journal of Botany93:860–867.

Anton, C., M. Musche, V. Hula, and J. Settele. 2008.Myrmicahost-ants limit the density of the ant-predatory large blue Maculinea nausithous. Journal of Insect Conservation12:511–517.

Armbruster, P., and D. H. Reed. 2005. Inbreeding depression in benign and stressful environments. Heredity 95:235–42.

Arnyas, E., J. Bereczki, A. Toth, K. Pecsenye, and Z. Varga. 2006. Egg-laying preferences of the xerophilous ecotype ofMaculinea alcon(Lepidoptera: Lycaenidae) in the Aggtelek National Park. European Journal of Entomology 103:587–595.

Arunkumar, R., T. I. Maddison, S. C. Barrett, and S. I. Wright. 2016. Recent mating-system evolution in Eichhornia is accompanied by cis-regulatory divergence. New Phytologist211:697–707.

Arunkumar, R., R. W. Ness, S. I. Wright, and S. C. Barrett. 2015. The evolution of selfing is accompanied by reduced efficacy of selection and purging of deleterious mutations. Genetics199:817–829.

Ashman, T. L., and C. J. Majetic. 2006. Genetic constraints on floral evolution: a review and evaluation of patterns. Heredity96:343–52.

Baker, H. G. 1955. Self-compatibility and establishment after "long distance" dispersal. Evolution9:347–349.

Baker, H. G., 1965. Characteristics and modes of origin of weeds. Pages 147–172inH. G. Baker and G. L.

Stebbins, editors. The genetics of colonizing species. Academic Press Inc., New York, USA.

Baldwin, I. T. 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences of the United States of America95:8113–

8118.

Barrett, S. C. 2003. Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond.

Philosophical Transactions of the Royal Society B-Biological Sciences358:991–1004.

Barrett, S. C. H. 2002. The evolution of plant sexual diversity. Nature Reviews: Genetics3:274–284.

Barrett, S. C. H., R. Arunkumar, and S. I. Wright. 2014. The demography and population genomics of evolutionary transitions to self-fertilization in plants. Philosophical Transactions of the Royal Society B-Biological Sciences 369.

Barrett, S. C. H., and L. D. Harder. 1996. Ecology and evolution of plant mating. Trends in Ecology &

Evolution11:73–79.

Barrett, S. C. H., L. D. Harder, and A. C. Worley. 1996. The comparative biology of pollination and mating in flowering plants. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 351:1271–1280.

Barros, M. A. G. E. 1996. Biologia reprodutiva e polinização de espécies simpátricas de Diplusodon (Lythraceae). Acta Botánica Mexicana37:11–21.

Bates, D., M. Maechler, B. Bolker, and S. Walker. 2014. lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-7 URL http://cran.r-project.org/web/packages/lme4/index.html.

Bellanger, S., J.-P. Guillemin, S. Touzeau, and H. Darmency. 2015. Variation of inbreeding depression in Centaurea cyanus L., a self-incompatible species. Flora - Morphology, Distribution, Functional Ecology of Plants212:24–29.

Berg, R. L. 1960. The ecological significance of correlation pleiades. Evolution14:171–180.

Bradshaw, H. D., S. M. Wilbert, K. G. Otto, and D. W. Schemske. 1995. Genetic mapping of floral traits associated with reproductive isolation in monkeyflowers (Mimulus). Nature376:762–765.

Bremer, B., K. Bremer, M. Chase, M. Fay, J. Reveal, D. Soltis, P. Soltis, and P. Stevens. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III.

Botanical Journal of the Linnean Society161:105–121.

100

Broz, A. K., A. M. Randle, S. A. Sianta, A. Tovar-Méndez, B. McClure, and P. A. Bedinger. 2017. Mating system transitions in Solanum habrochaites impact interactions between populations and species. New Phytologist 213:440–454.

Brunet, J. 1992. Sex allocation in hermaphroditic plants. Trends in Ecology & Evolution7:79–84.

Brunet, J., and H. R. Sweet. 2006. Impact of insect pollinator group and floral display size on outcrossing rate. Evolution60:234–246.

Buchmann, S. L. 1987. The ecology of oil flowers and their bees. Annual Review of Ecology and Systematics 18:343–369.

Burton, F. 1878. Gentiana asclepiadea and bees. Nature17:201–202.

Busch, J. W. 2005. The evolution of self-compatibility in geographically peripheral populations of Leaven-worthia alabamica (Brassicaceae). American Journal of Botany92:1503–1512.

Busch, J. W., and L. F. Delph. 2017. Evolution: selfing takes species down Stebbins’s blind alley. Current Biology 27:R61–R63.

Busch, J. W., S. Joly, and D. J. Schoen. 2011. Demographic signatures accompanying the evolution of selfing in Leavenworthia alabamica. Molecular Biology and Evolution28:1717–1729.

Busch, J. W., M. Neiman, J. M. Koslow, and S. Kalisz. 2004. Evidence for maintenance of sex by pathogens in plants. Evolution58:2584–2590.

Button, L., A. L. Villalobos, S. R. Dart, and C. G. Eckert. 2012. Reduced petal size and color associated with transitions from outcrossing to selfing inCamissoniopsis cheiranthifolia(Onagraceae). International Journal of Plant Sciences173:251–260.

Cariveau, D., R. E. Irwin, A. K. Brody, L. S. Garcia-Mayeya, and A. Von Der Ohe. 2004. Direct and indirect effects of pollinators and seed predators to selection on plant and floral traits. Oikos104:15–26.

Carleial, S., A. Delgado-Salinas, C. A. Domínguez, and T. Terrazas. 2015. Reflexed flowers inAeschynomene amorphoides (Fabaceae: Faboideae): a mechanism promoting pollination specialization? Botanical Journal of the Linnean Society177:657–666.

Chalcoff, V. R., and M. A. Aizen. 2016. Pollination unpredictability and ovule number in a South-Andean Proteaceae along a rainfall gradient. Australian Journal of Botany 64:8–14.

Charlesworth, D., and B. Charlesworth. 1987. Inbreeding depression and its evolutionary consequences.

Annual Review of Ecology and Systematics18:237–268.

Charlesworth, D., and J. H. Willis. 2009. The genetics of inbreeding depression. Nature Reviews Genetics 10:783–796.

Cheverud, J., G. P. Wagner, and M. M. Dow. 1989. Methods for the comparative analysis of variation patterns. Systematic Biology38:201–213.

Christensen, O. F., and P. J. Ribeiro Jr. 2015. geoRglm: a package for generalised linear spatial models. R package version 0.9-8 URLhttps://cran.r-project.org/web/packages/geoRglm/index.html.

Chung, A. Y., C. R. Maycock, E. Khoo, C. V. Khen, R. C. Kendrick, et al. 2011. New records of florivory on dipterocarp flowers. Malayan Nature Journal63:577–590.

Clark, D. B. 1985. Ecological field studies in the tropics: geographical origin of reports. Bulletin of the Ecological Society of America 66:6–9.

Clauss, M. J., and M. A. Koch. 2006. Poorly known relatives ofArabidopsis thaliana. Trends in Plant Science11:449–459.

Clegg, M. T. 1980. Measuring plant mating systems. Bioscience30:814–818.

Conner, J. K. 2002. Genetic mechanisms of floral trait correlations in a natural population. Nature 420:407–410.

Conner, J. K., and S. Rush. 1996. Effects of flower size and number on pollinator visitation to wild radish, Raphanus raphanistrum. Oecologia105:509–516.

Costelloe, B. H. 1988. Pollination ecology ofGentiana andrewsii. Ohio Journal of Science88:132–138.

Crnokrak, P., and D. A. Roff. 1999. Inbreeding depression in the wild. Heredity83:260–270.

Cruden, R. W. 1977. Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants.

Evolution31:32–46.

Darwin, C. 1876. The effects of cross and self fertilization in the vegetable kingdom. Murray, London.

Delpino, F. 1873-1874. Ulteriori osservazioni e considerazioni sulla dicogamia nel regno vegetale. Atti della Società Italiana di Scienze Naturali16:151–349.

Devries, P., R. Cocroft, and J. Thomas. 1993. Comparison of acoustical signals inMaculinea butterfly caterpillars and their obligate hostMyrmicaants. Biological Journal of the Linnean Society49:229–238.

Dlugosch, K. M., and I. M. Parker. 2007. Molecular and quantitative trait variation across the native range of the invasive species Hypericum canariense: evidence for ancient patterns of colonization via pre-adaptation? Molecular Ecology16:4269–4283.

Dlugosch, K. M., and I. M. Parker. 2008. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology 17:431–449.

Doubleday, L. A. D., R. A. Raguso, and C. G. Eckert. 2013. Dramatic vestigialization of floral fragrance across a transition from outcrossing to selfing in Abronia umbellata(Nyctaginaceae). American Journal of Botany100:2280–2292.

Eckert, C. G., and S. C. H. Barrett. 1994. Post-pollination mechanisms and the maintenance of outcrossing in self-compatible, tristylous,Decodon verticillatus (Lythraceae). Heredity72:396–411.

Eckert, C. G., S. Kalisz, M. A. Geber, R. Sargent, E. Elle, P.-O. Cheptou, C. Goodwillie, M. O. Johnston, J. K. Kelly, D. A. Moeller, et al. 2010. Plant mating systems in a changing world. Trends in Ecology &

Evolution25:35–43.

Eckhart, V. M. 1991. The effects of floral display on pollinator visitation vary among populations ofPhacelia linearis (Hydrophyllaceae). Evolutionary Ecology5:370–384.

102

Ellis, A. G., and S. D. Johnson. 2009. The evolution of floral variation without pollinator shifts inGorteria diffusa(Asteraceae). American Journal of Botany96:793–801.

Ellstrand, N. C., and D. R. Elam. 1993. Population genetic consequences of small population size:

implications for plant conservation. Annual Review of Ecology and Systematics 24:217–242.

Elmes, G., J. Thomas, and J. Wardlaw. 1991. Larvae ofMaculinea rebeli, a large-blue butterfly, and their Myrmica host ants: wild adoption and behaviour in ant-nests. Journal of Zoology223:447–460.

Elmes, G. W., O. Hammersted, J. Martin, J. Thomas, J. Van Der Made, et al. 1994. Differences in host-ant specificity between Spanish, Duch and Swedish populations of the endangered butterfly, Maculinea alcon (DENIS et SHIFF.)(Lepidoptera). Memorabilia Zoologica48:55–68.

Elmes, G. W., J. A. Thomas, J. C. Wardlaw, M. E. Hochberg, R. T. Clarke, and D. J. Simcox. 1998.

The ecology ofMyrmicaants in relation to the conservation ofMaculineabutterflies. Journal of Insect Conservation 2:67–78.

Emlen, S. T., and L. W. Oring. 1977. Ecology, sexual selection, and the evolution of mating systems.

Science197:215–223.

Engel, E. C., and R. E. Irwin. 2003. Linking pollinator visitation rate and pollen receipt. American Journal of Botany90:1612–1618.

Faegri, K., and L. van der Pijl. 1966. The principles of pollination ecology. Pergamon Press, Oxford, UK.

Fenster, C. B., W. S. Armbruster, P. Wilson, M. R. Dudash, and J. D. Thomson. 2004. Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution, and Systematics35:375–403.

Fenster, C. B., and K. Ritland. 1994. Evidence for natural selection on mating system in Mimulus (Scrophulariaceae). International Journal of Plant Sciences155:588–596.

Fiedler, K. 1998. Lycaenid-ant interactions of the Maculinea type: tracing their historical roots in a comparative framework. Journal of Insect Conservation 2:3–14.

Finley, A. O., and S. Banerjee. 2015. spBayes: univariate and multivariate spatial-temporal modeling. R package version 0.3-9 URLhttps://cran.r-project.org/web/packages/spBayes/index.html.

Fisher, R. A. 1941. Average excess and average effect of a gene substitution. Annals of Eugenics11:53–63.

Fishman, L., A. J. Kelly, J. H. Willis, and M. Noor. 2002. Minor quantitative trait loci underlie floral traits associated with mating system divergence in Mimulus. Evolution56:2138–2155.

Fornoni, J., M. Ordano, R. Pérez-Ishiwara, K. Boege, and C. A. Domínguez. 2015. A comparison of floral integration between selfing and outcrossing species: a meta-analysis. Annals of Botany 117:299–306.

Fournier, D., H. Skaug, J. Ancheta, J. Ianelli, A. Magnusson, M. Maunder, A. Nielsen, and J. Sibert.

1994. AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optimization Methods & Software 27:233–249.

Fox, C. W., and D. H. Reed. 2011. Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246–258.

Foxe, J. P., T. Slotte, E. A. Stahl, B. Neuffer, H. Hurka, and S. I. Wright. 2009. Recent speciation associated with the evolution of selfing inCapsella. Proceedings of the National Academy of Sciences of the United States of America106:5241–5245.

Foxe, J. P., M. Stift, A. Tedder, A. Haudry, S. I. Wright, and B. K. Mable. 2010. Reconstructing origins of loss of self-incompatibility and selfing in North American Arabidopsis lyrata: a population genetic context.

Evolution64:3495–510.

Frey, F. M., and M. Bukoski. 2014. Floral symmetry is associated with flower size and pollen production but not insect visitation rates inGeranium robertianum(Geraniaceae). Plant Species Biology 29:272–280.

Fürst, M. A., and D. R. Nash. 2010. Host ant independent oviposition in the parasitic butterflyMaculinea alcon. Biology Letters6:174–176.

Gadeberg, R. M. E., and J. J. Boomsma. 1997. Genetic population structure of the large blue butterfly Maculinea alconin Denmark. Journal of Insect Conservation1:99–111.

Galen, C. 1989. Measuring pollinator-mediated selection on morphometric floral traits: bumblebees and the alpine sky pilot, Polemonium viscosum. Evolution43:882–890.

Galen, C. 1999. Why do flowers vary? The functional ecology of variation in flower size and form within natural plant populations. Bioscience 49:631–640.

Galen, C., and M. Newport. 1987. Bumble bee behavior and selection on flower size in the sky pilot, Polemonium viscosum. Oecologia74:20–23.

Gerum, R. C., S. Richter, B. Fabry, and D. P. Zitterbart. 2016. ClickPoints: an expandable toolbox for scientific image annotation and analysis. Methods in Ecology and Evolution8:750–756.

Gibernau, M., D. Barabé, P. Cerdan, and A. Dejean. 1999. Beetle pollination ofPhilodendron solimoesense (Araceae) in French Guiana. International Journal of Plant Sciences160:1135–1143.

Glémin, S. 2003. How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57:2678–2687.

Goldberg, E. E., S. P. Otto, J. C. Vamosi, I. Mayrose, N. Sabath, R. Ming, and T.-L. Ashman. 2017.

Macroevolutionary synthesis of flowering plant sexual systems. Evolution 71:898–912.

Gómez, J. M. 2003. Herbivory reduces the strength of pollinator-mediated selection in the Mediterranean herb Erysimum mediohispanicum: consequences for plant specialization. The American Naturalist 162:242–256.

Gómez, J. M., J. Bosch, F. Perfectti, J. D. Fernandez, M. Abdelaziz, and J. P. Camacho. 2008. Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators. Proceedings of the Royal Society of London, Series B: Biological Sciences 275:2241–2249.

Gómez, J. M., and F. Perfectti. 2010. Evolution of complex traits: the case of Erysimumcorolla shape.

International Journal of Plant Sciences171:987–998.

Gómez, J. M., F. Perfectti, J. Bosch, and J. P. M. Camacho. 2009. A geographic selection mosaic in a generalized plant-pollinator-herbivore system. Ecological Monographs79:245–263.

104

Gómez, J. M., F. Perfectti, and J. P. M. Camacho. 2006. Natural selection onErysimum mediohispanicum flower shape: insights into the evolution of zygomorphy. American Naturalist 168:531–545.

Gómez, J. M., R. Torices, J. Lorite, C. P. Klingenberg, and F. Perfectti. 2016. The role of pollinators in the evolution of corolla shape variation, disparity and integration in a highly diversified plant family with a conserved floral bauplan. Annals of Botany117:889–904.

Goodwillie, C., S. Kalisz, and C. G. Eckert. 2005. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology, Evolution, and Systematics36:47–79.

Griffin, P. C., and Y. Willi. 2014. Evolutionary shifts to self-fertilisation restricted to geographic range margins in North AmericanArabidopsis lyrata. Ecology Letters17:484–490.

Grindeland, J. M., N. Sletvold, and R. A. Ims. 2005. Effects of floral display size and plant density on pollinator visitation rate in a natural population ofDigitalis purpurea. Functional Ecology19:383–390.

Griz, L. M. S., and I. C. S. Machado. 2001. Fruiting phenology and seed dispersal syndromes in caatinga, a tropical dry forest in the northeast of Brazil. Journal of Tropical Ecology17:303–321.

Guo, Y. L., J. S. Bechsgaard, T. Slotte, B. Neuffer, M. Lascoux, D. Weigel, and M. H. Schierup. 2009.

Recent speciation ofCapsella rubellafromCapsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck. Proceedings of the National Academy of Sciences of the United States of

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