Introgression and the evolution of selfing in Calyptridium monospermum (Portulacaceae)

Insect-mediated self-pollination evolved from outcrossing in two species of Calyptridium. Plants of C. umbellatum are selfpollinated by insects. Most populations of C. monospermum are outcrossing, but those sympatric with C. umbellatum have a complex of floral adaptations that encourage insect-mediated self-pollination very similar to that of C. umbellatum. Allopatric populations of C. umbellatum and C. monospermum have consistent and distinctive chromatographic patterns, but sympatric populations may have varied combinations of the chromatographic patterns of both species. These two species are separated by strong incompatibility barriers, but these barriers are weaker or even rarely nonexistent in some sympatric populations. Data from 35 populations suggest that, although C. umbellatum and C. monospermum. are mostly reproductively isolated from one another, introgression played an important role in the evolution of the many floral modifications inivolved in a change to insect-mediated selfpollination in C. monospermum. Calyptridium unbellatum (Torrey) Greene and C. monospermum Greene are closely related and partly sympatric rosette-forming perennial herbs of montane western North America (Hinton, 1975). Although both species have a basic flower morphology that could have evolved only as an adaptation for insect cross-pollination, the flowers of C. umbellatum have modifications that encourage insect-mediated self-pollination (Hinton, 1976). This species, characterized by flowers with white petals, yellow to red anthers, and a strong odor, is primarily pollinated by butterflies, flies, or beetles. Calyptridium monospermum is an outcrosser over most of its range. The flowers have rose-colored petals and anthers and a faint or undetectable odor and are primarily pollinated by bumblebees. However, in areas of sympatry with the selfing C. umbellatum, C. monospermum includes populations with white petals and a strong floral odor. These populations of C. monspermum are visited by much the same pollinators as C. umbellatum and have a complex of floral modifications that promote inbreeding, highly similar to that of C. umbellatum (Hinton, 1976). These similar floral modifications include: a reorientation of the styles and stamens bringing anthers and stigma within a flower closer together; anthesis over a shorter period of time, resulting in an inflorescence more crowded with 1 This paper is part of a doctoral dissertation submitted to the University of California, Berkeley. I am deeply grateful to Robert Ornduff, Lincoln Constance, and Grady Webster for help. 2iBiology, George Mason University, Fairfax VA 22030. This content downloaded from 157.55.39.153 on Mon, 19 Sep 2016 04:45:39 UTC All use subject to http://about.jstor.org/terms 86 SYSTEMATIC BOTANY [Volume 1 open flowers; a great increase in stigmatic surface area; increased pollen production; and greater synchrony between pollen presentation and stigma receptiveness. All these modifications increase the probability that pollen will be deposited on stigmas within the same flower or within the same inflorescence of these self-compatible plants when the inflorescence is disturbed by insect visitation (Hinton, 1976). Two hypotheses could explain the apparent parallel evolution of insectmediated self-pollination in populations of these two species: 1) populations of C. monospermum in sympatry with C. umbellatum are subject to the same selective pressures that promote insect-mediated self-pollination in that species and have independently evolved similar floral modifications without gene exchange. 2) The selfing modifications of C. monospermum populations are derived by introgression from C. umbellatum although these characteristics may be maintained by natural selection because of similar selective pressures. There are numerous examples of parallelism in floral characters, which are adaptations to similar pollinators, in organisms too distantly related for any conceivable gene exchange; for example, the red, tubular, scentless, highly nectariferous flowers adapted to hummingbird pollination in such unrelated species as Delphinium cardinale (Ranunculaceae) and Mimulus cardinalis (Scrophulariaceae) (Grant 8c Grant, 1968). The second hypothesis, gene exchange reinforced by selective pressure, must also be seriously considered. Heiser's studies of introgression in several species of Helianthus (reviewed in Heiser, 1961) suggest that adaptative characters have passed from one species to another even though hybrids are rare and mostly infertile. Hybridization data from Hinton (1975) indicate that C. monospermum and C. umbellatum are separated by strong incompatibility barriers but that these barriers are weaker or rarely nonexistent in some sympatric populations of these species. The purpose of this paper is to discuss chromotographic data bearing on the presence or absence of gene exchange between sympatric populations of C. monospermum and C. umbellatum and its relationship to the parallel evolution of reproductive biology in these species. These data were obtained from 17 field populations of C. monospermum and 18 of C. umbellatum (localities in Hinton, 1975). Leaves and inflorescences were assayed for phenolic and related substances by means of two-dimensional paper chromatography of methanolic extracts, a technique shown to be useful in detecting introgression between species -(Carter 8c Brehm, 1969). Fresh leaves and inflorescences, mass collected from plants of field populations of C. monospermum and C. umbellatum, were extracted separately in absolute methanol for several days at room temperature. Extracts were concentrated by evaporation under a vacuum at room temperature and spotted on Whatman No. 1 chromatographic paper (46 x 57 cm). Chromatographs were developed descendingly along the long axis with t-butanol, acetic acid, water (3:1:1,v/v/v), dried, This content downloaded from 157.55.39.153 on Mon, 19 Sep 2016 04:45:39 UTC All use subject to http://about.jstor.org/terms 1976] HINTON: INTROGRESSION IN CALYPTRIDIUM MONOSPERMUM 87 TABLE 1. Chromatographic spots (numbered 1 to 20) from extracts of flowers (Fl.) and leaves (Lf.) in populations (numbered in italics) of Calyptridium. Other Markers markers Chromatograph spots absent present C. monospermum, rose-petaled 1450 Fl. 1 2 3 4 5 6 7 8 9 10 -14 -none none Lf. --2 7 10 11 12 1453 Fl. 1 2 3 4 5 6 7 8 9 10 ----14 none none Lf. 2 --7 10 11 12 -------1459 Fl. 1 2 3 4 5 6 7 8 9 10 ---14 none none Lf. --2 2-7 -10 11 12 1472 Fl. 1 2 3 4 5 6 7 8 9 10 ----14 none none Lf. 2 --7 10 11 12 13 1488 Fl. 1 2 3 4 5 6 7 8 9 ----14 none none Lf. 2-7 ---11 12 13 1489 Fl. 1 2 3 4 5 6 7 8 9 10 ----14 none none Lf. 2 7 10 11 12 T-----____ 1492 Fl. 1 2 3 4 5 6 7 8 9 -----14 none none