Ontogenetic Differences in Heterostylous Plants and Implications for Development From a Herkogamous Ancestor

Abstract

Abstract. Alternative ontogenetic pathways among heterostylous species of Rubiaceae may reflect differences in their evolutionary histories. In this study, measurements were taken at different developmental stages on a series of longstyled (LS) and short-styled (SS) buds of the heterostylous taxa Psychotria chiapensis, P. poeppigiana, and Bouvardia ternifolia (all Rubiaceae). Results indicated that modifications in growth rates of stamens relative to corollas in all three species led to differences in anther heights between LS and SS flowers. Distinct style heights for LS and SS flowers of P. chiapensis and P. poeppigiana originate in the earlier stages of bud development and are maintained as styles elongate at equal rates. This contrasts with B. ternifolia, which has differences in style heights resulting from unequal relative growth rates between floral morphs. The ''approach herkogamous'' floral morphology, defined by having stigmas positioned above anthers, has been proposed as a potential evolutionary precursor for heterostylous taxa. To examine this hypothesis, floral development of two species with approach herkogamous morphologies, Psychotria pittieri and P. brachiata, was compared to that of the three heterostylous taxa. Differences in the relative rates of style elongation for flowers of approach herkogamous versus heterostylous species predict additional steps in the original model for the evolution of heterostyly from an approach herkogamous ancestor. The diversity of heterostylous ontogenies found within Rubiaceae provides insight into potential evolutionary pathways for this sexual system in other angiosperm families.Key words. Distyly, floral development, herkogamy, heterostyly, ontogeny, Psychotria, Rubiaceae.Received May 7, 1999. Accepted November 30, 1999 Studies of floral ontogeny have played a key role in our understanding of plant sexual system evolution (Diggle 1992) including studies of gynodioecy (Gibson and Diggle 1998), cleistogamy and chasmogamy (Lord 1982;Lord and Hill 1987), autogamy (Hill et al. 1992;Fenster et al. 1995), and heterostyly (Richards and Barrett 1984, 1992Richards and Koptur 1993). Convergent evolution of floral or reproductive form among closely related taxa has often been revealed by differences in developmental patterns (Guerrant 1982;Hufford 1988 Hufford , 1997Kellogg 1990;Friedman and Carmichael 1998).One goal of this study is to compare the heterostylous ontogeny of two congeneric and a more distantly related species to progress toward defining the degree of developmental variation among heterostylous species within a family (or evolutionary unit). Heterostyly is a sexual system in which plants of the same species produce one of two (distyly) or three (tristyly) floral morphs (Darwin 1877;Ganders 1979;Barrett 1990Barrett , 1992b. In a distylous species, individual plants produce either long-styled (LS) flowers with the stigma positioned above the anthers or short-styled (SS) flowers with the stigma positioned below the anthers (see Fig. 1), both of which occur ...

Floral Development at Multiple Spatial Scales in Polygonum jucundum (Polygonaceae), a Distylous Species with Broadly Open Flowers

“…Thus, the filament made little contribution to the anther height in these species [10], [16], [31]. However, in P. jucundum , the stamens are independent from the separate tepals and they possess long filaments.…”

“…It is thought that either the dimorphic height of floral organs evolves after the appearance of self-incompatibility in homostylous ancestor [13] or distylous taxa evolve from a self-compatible ancestor with a herkogamous floral morphology [6]. The evolutionary process of some distylous taxa has been revealed by investigations into the development of floral organs [10], [14]–[16]. In the floral development of these distylous species, four different development pathways are known to cause differences in stigma heights between LS and SS flowers.…”

“…Only two different development pathways are observed in the divergency of anther heights between two types of flowers. The relative growth rate of buds is very important in these two pathways [10], [16]–[19]. These developmental differences suggest that a stigma-height mutation is the probable cause of distyly and that the ancestors of these distylous taxa have “approach herkogamy” or “reverse herkogamy” with stigmas borne at a different level to the anthers [10], [16].…”

“…Although these floral development studies have helped us to understand the evolution of floral dimorph, they are limited to families that contain a corolla tube to which anthers adhere through a short filament [10], [14], [20]–[25]. However, some distylous flowers in other families are broadly open rather than narrowly tubular [26].…”

Phenotypic integration in style dimorphic daffodils (Narcissus, Amaryllidaceae) with different pollinators

“…An important aspect of Narcissus flowers is that the filaments are fused to the flower tube. Hence, the high correlations observed for anther position and flower tube length both in dimorphic and L-monomorphic populations might reflect important developmental constraints, genetic correlation and pleiotropy (see discussion above, [89][90][91]). However, we detected differences in the strength of correlations as predicted by Berg [2,18], and the results fitted the expectations that LT-pollinators exert stronger selection on anther position than ST-pollinators.…”