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An Increase in Atypical Petal Numbers During a Shift to Autogamy in a Coastal Sand Verbena And

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An Increase in Atypical Petal Numbers During a Shift to Autogamy in a Coastal Sand Verbena And bioRxiv preprint doi: https://doi.org/10.1101/2021.01.03.425117; this version posted January 4, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 1 An increase in atypical petal numbers during a shift to autogamy in a coastal sand verbena and 2 potential evolutionary mechanisms 3 Eric F. LoPresti1,2*; James G. Mickley3, Caroline L. Edwards1,4 & Marjorie G. Weber1 4 1: Dept. Plant Biology and Program in Ecology, Michigan State University 5 2: Dept. Plant Biology, Ecology, and Evolution, Oklahoma State University 6 3: Dept. of Botany and Plant Pathology, Oregon State University 7 4: Dept. of Biology, Indiana University 8 *Address for correspondence: [email protected] 9 10 Running title: Atypical flower production in Abronia umbellata 11 12 Manuscript received _______; revision accepted _______. 13 bioRxiv preprint doi: https://doi.org/10.1101/2021.01.03.425117; this version posted January 4, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 14 Abstract 15 Premise: 16 The evolution of variation in reproductive traits is of longstanding interest in biology. In plants, 17 meristic traits, such as petal and sepal numbers, are usually considered invariant within taxa. 18 However, certain species consistently exhibit great variability in these traits, though the factors 19 contributing to “atypical” counts are not well-known. The sand verbenas, Abronia 20 (Nyctaginaceae), usually have five perianth lobes (‘petals’) in their fused corollas and are self- 21 incompatible, thus departures from either of these norms in populations, varieties, or species are 22 of evolutionary interest. 23 Methods: 24 To characterize and understand an increase in atypical petal numbers during a transition from 25 xenogamy (outcrossing) to autogamy (selfing) in the coastal sand verbena Abronia umbellata, 26 we integrated common garden studies with analysis of over 11,000 photographed flowers from 27 iNaturalist, a citizen science project. Here we evaluate several adaptive and nonadaptive 28 explanations for the production of these ‘atypical’ flowers. 29 Key results 30 Our photo analysis and common garden show that the nominate xenogamous variety has 5 petals 31 with very little variation, however, an autogamous, geographically separated variety, A. u. var. 32 breviflora has a high preponderance of four-petalled morphs. Flower morph did not affect 33 successful autogamy, and petal numbers were not related to environmental factors, hybridization, 34 or flower size in the ways hypothesized. bioRxiv preprint doi: https://doi.org/10.1101/2021.01.03.425117; this version posted January 4, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 35 Conclusions 36 We conclude that this loss of petals is consistent with relaxation of selection on petal number in 37 selfers, inbreeding leading to a loss of developmental stability, or correlated selection on another 38 trait. This study strongly demonstrates the power of data available from public citizen databases 39 for easily scored traits, such as petal number. 40 41 Keywords: Abronia; autogamy; citizen science; floral traits, hybridization, iNaturalist, meristic 42 variation, Nyctaginaceae, petal number, 43 bioRxiv preprint doi: https://doi.org/10.1101/2021.01.03.425117; this version posted January 4, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 44 INTRODUCTION 45 Understanding variation in reproductive traits has long been a focus in evolutionary biology. 46 Taxonomic and geographic variation in reproductive phenotypes can provide key insights into 47 fundamental evolutionary processes such as selection, speciation, and adaptation. In plants, petal 48 number and other meristic characters are easily quantified reproductive traits. On one hand, these 49 characters are often considered fixed within species, genera, or families and, as such, are 50 commonly used in species descriptions, keys, and other taxonomic and identification resources. 51 Any departure from a ‘normal’ meristic character within a taxon, whether species, genus, or even 52 family, is thus of evolutionary, developmental, morphological, and taxonomic interest (Ellstrand, 53 1983). On the other hand, interspecific transitions in petal number or intraspecific variants in 54 petal number are quite common in wild plants of many families, and may take the form of a 55 change in mean or variance within or among species (e.g. Stark, 1918; Lowndes, 1931; 56 Saunders, 1934; Roy, 1962; Huether, 1968; Schemske, 1978; Ellstrand, 1983; Lehmann, 1987; 57 Shepard et al., 2005). Despite interest in the development, breeding, genetics, and evolution of of 58 meristic variation, critical examination of evolutionary drivers of patters of variation, whether 59 adaptive or non-adaptive, are scarce. Here, we integrate lab, field, and citizen-science data to 60 examine support for several a priori hypotheses (Table 1) about patterns of petal number 61 variation using a coastal sand verbena (Abronia umbellata, Nyctaginaceae) where allopatric 62 varieties show remarkably different patterns of variation in perianth lobe (hereafter petal, as 63 functionally equivalent) number. 64 Several hypotheses concern petal number evolution in plants, broadly falling into adaptive and 65 non-adaptive categories. The invariance of petal number, notably across many taxa in the 66 ancestrally five-petalled Pentapetalae (a group which includes much of Eudicot diversity: bioRxiv preprint doi: https://doi.org/10.1101/2021.01.03.425117; this version posted January 4, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 67 Cantino et al., 2007; Soltis and Soltis, 2013), suggests a highly conserved developmental 68 program (Endress 2001), or selection maintaining constancy (Stebbins, 1974; Herrera, 2009). If 69 the mechanism is selective, pollinator choice or innate preference would be obvious candidates 70 for the maintenance of petal number. While pollinator selection has been long-hypothesized (e.g. 71 Leppik, 1953), positive evidence for this hypothesis remains elusive. Certain pollinators may 72 have the capability to ‘count’ petals, though many others were not found to differentiate petal 73 numbers (e.g., Leppik, 1953; Golding et al., 1999; Mickley, 2017). In this vein, Mickley and 74 Schlichting (2018) devised an alternate way of examining pollinator-mediated stabilizing 75 selection on petal number. They reasoned that if pollinators were maintaining a fixed petal 76 number, autogamous species would lack constancy due to relaxed selection on petal number. 77 Using several closely-related species of Polemoniaceae, they found no evidence that 78 xenogamous species had greater constancy in petal number than autogamous congeners. 79 However, using many species in a comparative phylogenetic analysis would be necessary to 80 robustly test this hypothesis. 81 An alternative, but related, hypothesis is that loss of petals in autogamous taxa may be adaptive, 82 but unrelated to pollinator preferences, if petals are costly (e.g., Galen, 1999; Strauss & Whittall, 83 2007; Lambrecht 2013) or if loss of petals increases autogamous efficiency. The autogamous 84 efficiency hypothesis was formulated by Monnaiux et al. (2016) as a potential mechanism by 85 which Cardame hirsuta, an autogamous mustard, has reduced petals from the four-petals typical 86 of Brassicaceae. Specifically, they hypothesize that petal loss slows bud opening and promotes 87 more effective selfing, though they do not test the proposed hypothesis (Table 1: H1). However, 88 a later paper found that a genotype with reduced petal numbers had a lower outcrossing rate in 89 the field, but did not differ in seed set in the lab (Monnaiux et al., 2018). Therefore, it is unlikely bioRxiv preprint doi: https://doi.org/10.1101/2021.01.03.425117; this version posted January 4, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 90 that low petal number increased autogamous success in C. hirsuta, as hypothesized, but this 91 intriguing hypothesis certainly deserves testing in other plant species. 92 Non-adaptive evolutionary or phenomenological hypotheses have also been proposed to drive 93 petal number variation. For example, inbreeding itself, independent of pollinator-mediated 94 selection could reduce meristic stability (Table 1: H2). Another set of non-adaptive hypotheses 95 focus on hybridization. Hybridization, especially between distantly-related taxa, may cause 96 breakdown in the canalization
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