The Effects of Flower Color Transitions on Diversification Rates in Morning Glories (Ipomoea Subg

University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications in the Biological Sciences Papers in the Biological Sciences 1-1-2010 The ffecE ts of Flower Color Transitions on Diversification Rates in Morning Glories (Ipomoea subg. Quamoclit, Convolvulaceae) Stacey DeWitt mithS University of Nebraska - Lincoln, [email protected] Richard E. Miller Southeastern Louisiana University, [email protected] Sarah P. Otto University of British Columbia, [email protected] Richard G. FitzJohn University of British Columbia, [email protected] Mark D. Rausher Duke University, [email protected] Follow this and additional works at: http://digitalcommons.unl.edu/bioscifacpub Part of the Life Sciences Commons Smith, Stacey DeWitt; Miller, Richard E.; Otto, Sarah P.; FitzJohn, Richard G.; and Rausher, Mark D., "The Effects of Flower Color Transitions on Diversification Rates in Morning Glories (Ipomoea subg. Quamoclit, Convolvulaceae)" (2010). Faculty Publications in the Biological Sciences. Paper 123. http://digitalcommons.unl.edu/bioscifacpub/123 This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications in the Biological Sciences by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Published in M. Long, H. Gu, & Z. Zhou, eds., Darwin’s Heritage Today: Proceedings of the Darwin 200 Beijing International Conference (Beijing, China: Higher Education Press, 2010), pp. 202–226. The Effects of Flower Color Transitions on Diversification Rates in Morning Glories (Ipomoea subg. Quamoclit, Convolvulaceae) Stacey D. Smith,1 Richard E. Miller,2 Sarah P. Otto,3 Richard G. FitzJohn,3 and Mark D. Rausher 1 1. Department of Biology, Box 90338, Duke University, Durham, North Carolina, USA 2. Department of Biological Sciences, Southeastern Louisiana University, Hammond, Louisiana 70402, USA 3. Department of Zoology and Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada Corresponding author — Mark D. Rausher, tel 919 684-2295, fax 919 660-7293, email [email protected] Abstract As in many clades of flowering plants, the Quamoclit clade of morning glories (Ipomoea subgenus Quamoclit) ex- hibits unequal proportions of different flower colors, with pigmented species outnumbering unpigmented species by nearly a factor of 7. We examined three possible macroevolutionary explanations for this pattern: (1) asymmetric transition rates between pigmented and unpigmented flowers; (2) low transition rates preventing the flower colors from reaching equilibrium; and (3) differential diversification. In order to discriminate among these explanations, we employ the newly-developed Binary-State Speciation and Extinction (BiSSE) model, which jointly estimates transition rates among states and the speciation and extinction rates in each state. Us- ing maximum likelihood and Bayesian BiSSE estimation, we find no evidence for asymmetrical transition rates. Also, BiSSE simulations of character evolution demonstrate that there is sufficient time for the estimated transition rates to produce as many or even more white species than we observe in Quamoclit, suggesting that low- transition rates do not fully account for the paucity of white species. In contrast, we find support for the differential diversification hypothesis with the rate of speciation in pigmented lineages estimated as three-fold greater than the rate in unpigmented lineages. Our analyses thus indicate the low frequency of white-flowered morning glory species is due largely to lineage selection. Our analysis also suggests that estimating character transition rates without simultaneously estimating speciation and extinction rates can lead to greatly biased estimates of transition rates. Keywords: Anthocyanins, diversification, Ipomoea, transition rate Introduction form of group selection, but he wrote little about selection at other levels. Because he knew nothing In On the Origin of Species, as well as in his other about the mechanisms of inheritance, he did not works, Darwin wrote extensively about evolution- conceive of meiotic drive, segregation distortion, ary changes within lineages and their causes. As is or selfish genetic elements. At higher levels, he ap- well-known, the mechanisms he described were fo- pears to have given little attention to the possibility cused on individuals (in the case of natural selec- of lineage selection. tion) or on mating pairs (in the case of sexual se- In the 150 years since The Origin, it has become lection). In his discussion of the evolution of neuter clear that selection at levels below and above the castes of social insects, he did however propose a individual do occur (Lewontin 1970; Hurst and 205 206 S. D. SMITH ET AL. IN DARWIN’S HERITAGE TODAY (2010) Werren 2001; Jablonski 2008). In particular, at achieves an equilibrium distribution of flower col- higher levels, there are many reported examples ors (Nosil and Mooers 2005; Maddison 2006). If, of differential lineage extinction or speciation in- for example, purple flowers were more likely to volving both individual characters and emergent change to red flowers than the reverse, red-flow- characters of populations or species (Jablonski ered species would eventually come to outnum- 2008; Rabosky and McCune 2009). But while lin- ber purple-flowered species, or even replace them eage selection is an accepted phenomenon, its con- entirely. Such asymmetrical transition rates could sequences for macroevolutionary patterns are still arise due to genetic constraints or to selective poorly understood. In this report, we focus on one forces that favor transitions in one direction but macroevolutionary pattern that is potentially influ- not in the reverse (Zufall and Rausher 2004). enced by lineage selection: the proportion of spe- A second macroevolutionary factor is low rates cies within a clade exhibiting a particular state of of transition between flower-color states. In par- a character of interest. As we describe below, this ticular, if transition rates between flower colors proportion is expected to be determined, on the are equal but low relative to the rate of diversifi- one hand, by rates of evolutionary transitions be- cation, we would expect that most species would tween character states, and on the other hand, by retain the ancestral state for the group as opposed state-specific extinction and speciation rates. Here to reaching the equilibrium of equal numbers we seek specifically to understand the relative im- of species in each state (Schwander and Crespi portance of differential speciation, extinction and 2009). Thus, if having pigmented flowers were the transition rates in the evolution of an ecologically ancestral state in penstemons, the rarity of white important trait: flower color. species might be attributed to a low rate of change Flower color is evolutionarily very labile. For to white. example, many species exhibit natural polymor- A third factor potentially contributing to dif- phisms in flower color (e.g. Jones and Reithel 2001; ferences in flower colors among species in a clade Zufall and Rausher 2003; Streisfeld and Kohn is differential diversification. If increased specia- 2005). Above the species-level, it is frequently the tion or decreased extinction is associated with lin- case that sister taxa differ markedly in flower color eages with particular flower colors, those col- (Campbell et al. 1997; Wesselingh and Arnold 2000; ors will become more common than species with Porter et al. 2009; Wilson 2004). Despite this wide- other colors. Flower color transitions are often as- spread capacity for flower color evolution, partic- sociated with adaptations to new environments ular colors often account for a disproportionately or new pollinators, potentially resulting in a shift large or small number of species in a given group in diversification rates (Dodd et al. 1999; Fenster (Perret et al. 2003; Tripp and Manos 2008). For ex- et al. 2004; Strauss and Whittall 2006). The nectar ample, among the estimated 270 species of penste- spurs of Aquilegia are a classic example of this phe- mons, only 6 are white-flowered (Lodewick and nomenon, where the transition from unspurred Lodewick 1999; Wilson et al. 2004), and similarly, to spurred flowers resulted in increased diversifi- only 5 of the 70 species of Phlox produce exclu- cation (Hodges and Arnold 1995). This effect has sively white flowers (Wherry 1955). While the rep- been attributed to the potential for reproductive resentation of different flower colors in a clade is isolation between populations or species differ- likely to vary by pure chance, there also are macro- ing in spur length (Whittall and Hodges 2007). A evolutionary factors that may account for the dif- similar scenario could be envisioned with flower ferential species richness. color. For example, the transition from pigmented One such factor is an asymmetry in rates of tran- to white flowers could allow exploitation of a new sition between flower color states. Assuming no and diverse group of pollinating moths, and trig- net differences in the diversification of species with ger an increase in speciation associated to special- different colors, the flower color state that is most ization for different moth species (see Sargent 2004 likely to change is expected to be rare once a clade for evidence of

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