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Extreme Environments Select for Reproductive Assurance: Evidence from Evening Primroses (Oenothera) Margaret E.K

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Extreme Environments Select for Reproductive Assurance: Evidence from Evening Primroses (Oenothera) Margaret E.K University of Connecticut OpenCommons@UConn EEB Articles Department of Ecology and Evolutionary Biology 2011 Extreme environments select for reproductive assurance: evidence from evening primroses (Oenothera) Margaret E.K. Evans Museum National d'Histoire Naturelle David J. Hearn Towson University Kathryn E. Theiss University of Connecticut - Storrs, [email protected] Karen Cranston National Evolutionary Synthesis Center Kent E. Holsinger University of Connecticut - Storrs, [email protected] See next page for additional authors Follow this and additional works at: https://opencommons.uconn.edu/eeb_articles Part of the Botany Commons, and the Evolution Commons Recommended Citation Evans, Margaret E.K.; Hearn, David J.; Theiss, Kathryn E.; Cranston, Karen; Holsinger, Kent E.; and Donoghue, Michael J., "Extreme environments select for reproductive assurance: evidence from evening primroses (Oenothera)" (2011). EEB Articles. 24. https://opencommons.uconn.edu/eeb_articles/24 Authors Margaret E.K. Evans, David J. Hearn, Kathryn E. Theiss, Karen Cranston, Kent E. Holsinger, and Michael J. Donoghue This article is available at OpenCommons@UConn: https://opencommons.uconn.edu/eeb_articles/24 1 2 3 4 Extreme environments select for reproductive assurance: 5 evidence from evening primroses ( Oenothera ) 6 7 8 9 Margaret E. K. Evans 1, 2, 3 10 David J. Hearn 4 11 Kathryn E. Theiss 5 12 Karen Cranston 6 13 Kent E. Holsinger 5 14 Michael J. Donoghue 3 15 16 17 1 Author for correspondence 18 19 2 Current address: 20 Origin, Structure, and Evolution of Biodiversity UMR 7205 21 Museum National d’Histoire Naturelle 22 16 rue Buffon 23 75231 Paris cedex 05 24 [email protected] 25 (+33)140793366 (ph) 26 (+33)140793342 (fax) 27 28 29 30 3 Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 31 06511 32 4 Department of Biological Sciences, Towson University, 8000 York Road, Towson, MD 33 21252 34 5 Department of Ecology and Evolutionary Biology, University of Connecticut, 75 N. 35 Eagleville Road, 36 U-3043, Storrs, CT 06269 37 6 National Evolutionary Synthesis Center, 2024 W. Main Street, A200, Durham, NC 27705 38 39 40 41 Total word count: 3,894 42 Introduction: 774 43 Materials and Methods: 1,181 44 Results: 548 45 Discussion: 1,197 46 Acknowledgements: 81 1 47 1 Table, 2 Figures 48 Supporting Information: 1 Table 2 49 Summary 50 51 • Competing evolutionary forces shape plant breeding systems (e.g. , inbreeding 52 depression, reproductive assurance). Which of these forces prevails in a given 53 population or species is predicted to depend upon such factors as life history, 54 ecological conditions, and geographical context. Here we examined two such 55 predictions: that self-compatibility should be associated with (1) the annual life 56 history or (2) extreme climatic conditions. 57 • We analyzed data from a clade of plants remarkable for variation in breeding 58 system, life history and climatic conditions ( Oenothera , sections Anogra and 59 Kleinia , Onagraceae). We used a phylogenetic comparative approach and 60 Bayesian or hybrid Bayesian tests to account for phylogenetic uncertainty. GIS- 61 based climate data and ecological niche modeling allowed us to quantify 62 climatic conditions. 63 • Breeding system and reproductive lifespan are not correlated in Anogra +Kleinia . 64 Instead, self-compatibility is associated with the extremes of temperature in the 65 coldest part of the year and precipitation in the driest part of the year. 66 • In the 60 years since this pattern was anticipated, this is the first demonstration of 67 a relationship between the evolution of self-compatibility and climatic extremes. 68 We discuss possible explanations for this pattern and possible implications with 69 respect to anthropogenic climate change. 70 71 3 72 Key words: Baker’s Law, climate, evolution, life history, Oenothera , plant breeding 73 system, reproductive assurance, self-compatibility 4 74 Introduction 75 Puzzling over variation and evolution of plant breeding systems has occupied 76 some of the greatest thinkers of evolutionary biology (Darwin, 1876; Fisher, 1941; 77 Dobzhansky, 1950; Stebbins, 1950, 1957). A central pattern of interest is variation in 78 inbreeding vs. outbreeding, which is thought to arise from competing evolutionary 79 forces. On one hand, the negative fitness consequences of inbreeding (known as 80 inbreeding depression) favor outbreeding (Nagylaki, 1976; Lande & Schemske, 1985; 81 Charlesworth and Charlesworth, 1987). In many plants, self-incompatibility enforces 82 outcrossing, so that self-fertilization, the most extreme form of inbreeding, is impossible. 83 Phylogenetic analyses suggest that there have been relatively few origins of self- 84 incompatibility in seed plants (Weller et al., 1995; Igic & Kohn, 2001; Steinbachs & 85 Holsinger, 2002; Igic et al., 2008), whereas change to self-compatibility is described as 86 the most common evolutionary transition experienced by flowering plant lineages 87 (Stebbins, 1974). On the other hand, self-compatibility can be advantageous if it 88 provides “reproductive assurance”: a plant that finds itself without mates or pollinators 89 may still be able to reproduce (Darwin, 1876; Lloyd, 1979, 1992; Fausto et al., 2001; 90 Weber & Goodwillie, 2009). These two selective factors, inbreeding depression and 91 reproductive assurance, are thought to be among the most important acting on plant 92 breeding systems (Lloyd, 1979; Holsinger, 1996, 2000; Eckert et al., 2006). 93 Which of these competing forces wins out in shaping the breeding system of a 94 particular species or population is context-dependent, including factors such as life 95 history, ecological conditions, and geographical context. For example, it’s thought that 96 selection for reproductive assurance should be stronger in plants that have just one 97 opportunity to reproduce in their lifetime (annuals, monocarpic perennials) compared 5 98 to plants that have several chances to reproduce (polycarpic perennials; Morgan & 99 Schoen, 1997; Morgan, 2001). Thus annuals should be more likely than perennials to 100 evolve self-compatibility, whereas perennials should be more likely to retain self- 101 incompatibility (Stebbins, 1950; pp 176-181). This prediction has been borne out in some 102 surveys of plant breeding systems (Barrett et al., 1996) but not others (Raven, 1979). 103 Ecological conditions are also thought to modify selection on plant breeding 104 systems. Insect pollinator abundance can be low under cold conditions, i.e. , at high 105 elevations and latitudes, which might increase selection for reproductive assurance in 106 the plants found there (Moldencke, 1979; Kalin Arroyo, 1985; Korner, 1999; but see 107 Garcia-Camacho & Totland, 2009). Extremely arid conditions are associated with 108 variation in reproductive success (Beatley, 1974; Kadmon & Schmida, 1990; Philippi, 109 1993; Clauss & Venable, 2000; Schemske & Bierzychudek, 2001), which may generate 110 selection for reproductive assurance. Stebbins (1950) generalized this by suggesting 111 that extreme conditions should favor the evolution of selfing: “selection in favor of self- 112 fertilization is very likely to occur in all annuals and other short-lived plants living in 113 deserts, alpine or arctic regions, or other extreme environments”. Lloyd (1992) made a 114 similar association between environmental conditions (extreme temperatures, high 115 latitudes and altitudes) and selfing. 116 Here we evaluate patterns of covariation and coevolution of reproductive 117 lifespan (annual vs. iteroparous perennial), breeding system, and climatic conditions in 118 a clade of plants found in Western North America: Oenothera sections Anogra and 119 Kleinia (Onagraceae). This group of 19 taxa is remarkable for variation in climatic 120 conditions, life history, and breeding system (Table 1). Some of the Anogra +Kleinia taxa 121 are found in low-elevation deserts of the southwestern U. S., others in semi-arid 6 122 grasslands, and others in alpine meadows in the Rocky Mountain region (Wagner et al., 123 2007; Evans et al., 2009). Ten of the Anogra +Kleinia taxa are self-incompatible, four are 124 polymorphic in breeding system (either among or within populations), and five are self- 125 compatible (Klein, 1970; Raven, 1979; Theiss et al., 2010). In this same group, ten are 126 perennial, two are variable in life history, and seven are annual (Klein, 1970; Evans et al., 127 2005; Wagner et al., 2007). This variation makes the Anogra +Kleinia clade an excellent 128 group in which to evaluate coevolution of (1) breeding system and reproductive 129 lifespan and (2) breeding system and climate. We use a molecular phylogenetic 130 comparative approach to account for non-independence of taxa. Because of the 131 young age of the Anogra +Kleinia radiation (crown date within the last one million years; 132 Evans et al., 2009), there is considerable phylogenetic uncertainty (see Fig. 1a), which 133 we account for using a sample from the posterior distribution of Bayesian phylogenetic 134 trees. We use GIS-based climate data and ecological niche modeling to quantify the 135 climatic conditions where the Anogra +Kleinia taxa are found. Using the combination of 136 phylogenetic hypotheses, trait data, and climatic niche estimates, we evaluate the 137 predictions that (1) the perennial habit should be associated with self-incompatibility 138 and the annual habit with self-compatibility and (2) self-compatibility should be 139
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