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Developmental Variation and Distyly in Hedyotis Caerulea (Rubiaceae)

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Developmental Variation and Distyly in Hedyotis Caerulea (Rubiaceae) Cleveland State University EngagedScholarship@CSU Biological, Geological, and Environmental Biological, Geological, and Environmental Faculty Publications Sciences Department 2013 Developmental Variation and Distyly in Hedyotis caerulea (Rubiaceae) Dennis A. Sampson Cleveland State University Robert A. Krebs Cleveland State University, [email protected] Follow this and additional works at: https://engagedscholarship.csuohio.edu/scibges_facpub Part of the Plant Biology Commons How does access to this work benefit ou?y Let us know! Publisher's Statement Open Access Recommended Citation Sampson, D. A. and R. A. Krebs. 2013. Developmental variation and distyly in Hedyotis caerulea (Rubiaceae). SpringerPlus 2(1) http://dx.doi.org/10.1186/2193-1801-2-383. This Article is brought to you for free and open access by the Biological, Geological, and Environmental Sciences Department at EngagedScholarship@CSU. It has been accepted for inclusion in Biological, Geological, and Environmental Faculty Publications by an authorized administrator of EngagedScholarship@CSU. For more information, please contact [email protected]. Sampson and Krebs SpringerPlus 2013, 2:383 http://www.springerplus.com/content/2/1/383 a SpringerOpen Journal RESEARCH Open Access Developmental variation and the evolution of distyly in Hedyotis caerulea (Rubiaceae) Dennis A Sampson and Robert A Krebs* Abstract The development of distyly is thought to arise from differential growth patterns in the pin and thrum morphs. However, few detailed studies exist on the early floral development of distylous flowers, and fewer still look at variation in these traits among populations. Buds at multiple stages of development were collected from five populations of Hedyotis caerulea to quantify how pins and thrums diverge with respect to the initiation, rate, and termination of growth between the stamens and stigmas. The growth rate of anthers varied little spatially across five populations and temporally in both pins and thrums, although thrum anthers grew faster than pin anthers. Dimorphy in stigma height was more complex. Pin stigmas first grew at a faster rate than those of thrums, and late in bud development, growth of thrum styles slowed. These rate changes varied among populations, and they differed from the congeneric H. salzmanii. Similar differences between morphs are known in other heterostylous species, and such variation in growth pattern among related species has been used to infer independent evolution of distylous systems. Keywords: Bluets; Flowers; Herkogamy; Heterostyly; Houstonia; Isoplethy; Floral morphology Introduction that variation in floral organ development among families Morphological variation in flowers is determined by the derives from independent evolutionary events that led to combined effects of genotype, developmental program- tristyly. While they predicted that the same could be true ming, and environmental variation (Diggle 1992). Not for distyly, they lacked information on distylous floral de- surprisingly then studies of floral development have made velopment in a sufficient number of species largely limited significant contributions to understanding the evolution to members of the Boraginaceae (Cohen et al., 2012), of plant mating systems. When available, phylogenetic hy- Linaceae (Armbruster et al. 2006), Primulaceae (Stirling potheses concerning the taxa studied can be merged with 1932; Webster and Gilmartin 2006), Santalaceae (Riveros variation in their developmental patterns to identify pos- et al. 1987), and finally the Rubiaceae, which may be the sible evolutionary pathways by which new morphologies best studied family based on reports for Faramea emerge (e.g., Guerrant 1982; Hufford 1995; Kellogg 1990; suerrensis (Richards and Barrett 1992), Guettarda scabra Friedman and Carmichael 1998; Cohen 2011). With re- (Richards and Koptur 1993), Hedyotis salzmannii (Riveros spect to herkogamy and one stably polymorphic form, et al. 1995), Psyochotria spp and Bouvardia ternifolia distyly, understanding evolutionary change has been ham- (Faivre 2000), and Palicourea padifolia (Hernandez and pered by a need to track developmental change in floral Ornelas 2007). development (Cohen et al. 2012). A limited number of distylous species have been stud- Fewer than 20 papers during the last 100 years have crit- ied given that distyly occurs in some 28 different families ically examined how the different forms of flowers arise in (Barrett 2002). At least four distinct developmental path- heterostylous species according to Cohen (2010), who ways have been characterized for achieving differences noted that the majority of them focus on tristylous spe- in stigma height between pin (long-styled) and thrum cies. In one review, Richards and Barrett (1992) concluded (short-styled) flowers, and at least two developmental patterns contribute to differences in anther height be- * Correspondence: [email protected] tween the morphs (Faivre 2000; Cohen 2010). It is there- Department of Biological, Geological, and Environmental Sciences, Cleveland fore likely that additional developmental pathways will State University, 2121 Euclid Ave, Cleveland, OH 44115-2406, USA © 2013 Sampson and Krebs; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Sampson and Krebs SpringerPlus 2013, 2:383 Page 2 of 6 http://www.springerplus.com/content/2/1/383 be identified, and such variation among species as well Materials and methods as divergence among populations may help to establish We collected 212 pin buds and 219 thrum buds at vari- what evolutionary patterns most likely underlie the ori- ous stages of development from five populations of H. gins of this trait. caerulea in northeastern Ohio in May 2008: #2, 4, 9, 10 Here we quantitatively compared the initiation, rate, and 13 from Sampson and Krebs (2012), which will be and termination of growth between the stamens and identified here as A-E, respectively. Buds were chosen in stigmas in another member of the Rubiaceae, the a manner that included the widest range of development distylous Hedyotis caerulea, and make these measure- possible, although the smallest buds were selected first ments across multiple populations. The goal was to in order to ensure their adequate representation in the establish developmentally when and how the floral data set given that H. caerulea possess a short growing morphology of pins and thrums diverged, to compare season (Ornduff 1980). Tiny buds were chosen from development to a congener and other distylous taxa, plants that already had a mature flower, which is neces- and to produce inferences on the mechanisms by which sary to score the individual as a pin or a thrum. All buds distyly evolved. were preserved when fresh cut in 80% ethanol. Buds thrum 2.5 ABpin 2.0 y=0.56x + 0.10 y=0.58x + 0.13 r2 = 0.89 r2 = 0.95 1.5 1.0 0.5 y=0.27x + 0.25, r2 = 0.83 y=0.30x + 0.25, r2 = 0.85 0.0 2.5 C D 2.0 y=0.54x + 0.17 y=0.54x + 0.14 r2 = 0.94 r2 = 0.95 1.5 1.0 0.5 y=0.32x + 0.18, r2 = 0.93 y=0.34x + 0.19, r2 = 0.91 Anther Height (mm) 0.0 2.5 E F 2.0 y=0.56x + 0.15 y=0.56x + 0.13 r2 = 0.98 r2 = 0.94 1.5 1.0 0.5 y=0.32x + 0.23, r2 = 0.84 y=0.31x + 0.22, r2 = 0.86 0.0 0 0.5 1 1.5 2 2.5 3 3.5 0 0.5 1 1.5 2 2.5 3 3.5 Bud Length (mm) Figure 1 Anther development in pin and thrum floral morphs of H. caerulea. Data of bud lengths (mm) versus height of anthers (mm) were plotted for each bud collected across five populations (A-E), and F provides results for all populations combined, and lines of best fit are simple linear regression of bud length predicting anther height. Sampson and Krebs SpringerPlus 2013, 2:383 Page 3 of 6 http://www.springerplus.com/content/2/1/383 were dissected to measure bud length, stigma height, both a linear and a second-order term in models to test and anther height using an Olympus SZX12 dissecting whether the relationship could best be described as microscope equipped with an ocular micrometer accur- curvilinear or linear, and to improve the power of this par- ate to <0.01 mm at 90×, its highest resolution. ticular test, results of all five populations were pooled. Re- Bud length was examined as a relative estimate of lationships among populations were tested in general developmental time to which stigma height and anther linear models (Proc GLM; SAS Institute 2002) to assess height were compared in pin and thrum morphs. Bud size variation among populations as fixed factors and to test was the independent variable and floral organ measure- interactions between morphs and populations on both an- ments were the dependent variables, and both were log- ther and stigma height. transformed prior to regression analyses to normalize data under the assumption that variance correlates with the Results mean. Raw measurements, however, were also presented Variation in growth rate between pins and thrums for clarity and contrast. Size of developing stigmas and occurred very early in development (Figures 1 and 2). anthers were contrasted against total bud length using Across the five populations sampled, the linear term pin 2.5 A thrum B 2.0 y=0.87x - 0.14 y=0.70x + 0.14 r2 = 0.89 r2 = 0.87 1.5 1.0 0.5 y=0.43x + 0.12, r2 = 0.78 y=0.44x + 0.14, r2 = 0.79 0.0 2.5 C D 2.0 y=0.77x + 0.02 y=0.77x + 0.08 2 2 1.5 r = 0.93 r = 0.81 1.0 0.5 0.0 y=0.35x + 0.24, r2 = 0.78 y=0.50x + 0.05, r2 = 0.83 Stigma Height (mm) 2.5 E F 2.0 y=0.82x - 0.17 y=0.77x + 0.01 2 2 1.5 r = 0.86 r = 0.85 1.0 0.5 0.0 y=0.61x - 0.12, r2 = 0.91 y=0.45x + 0.09, r2 = 0.81 0 0.5 1 1.5 2 2.5 3 3.5 0 0.5 1 1.5 2 2.5 3 3.5 Bud Length (mm) Figure 2 Stigma development in pin and thrum floral morphs of H.
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