Persistent Habitat Instability and Patchiness, Sexual Attraction, Founder Events, Drift and Selection: A Recipe for Rapid Diversification of Orchids

Abstract

Orchidaceae is one of the most species-rich families of flowering plants, with most current diversity having evolved within the last 5 My. Patterns associated with species richness and rapid diversification have been identified but have not often been associated with evolutionary processes. We review the most frequently identified correlates of diversity and suggest that the processes and rate by which they occur vary geographically and are largely dependent on persistent pulses of habitat instabilities, especially for epiphytes. Aggressive orogenesis creates fragmented habitats while global climatic cycles exacerbate the ecological instabilities. The need for repeated cycles of dispersal results in frequent founder events, which sets the stage for allopatric diversification via bouts of genetic drift and natural selection. The allopatry requirement can be bypassed by pollination systems involving flowers attracting pollinators through the production of sex signaling semiochemicals. The drift-selection model of diversification, coupled with persistent habitat instability throughout ecological and geological time scales, and sex signaling are the likely components of a multifactorial process leading to the rapid, recent diversification in this family.

Keywords: Orchidaceae; dispersal; diversification rates; drift–selection model; epiphytism; founder events; habitat instability; mycorrhizal fungi; recent orogenesis; species richness.

Figure 1

Northern Andes, a region of high species richness and high diversification rates. (A) Eastern Andean Ridge in northern Peru, where the Andes and the Amazon meet. (B) Terrestrial Pterichis macroptera flowering among bunch grasses and rosettes of Puya (Bromeliaceae) in a high-Andean grassland (jalca), northern Peru. (C) Erycina glossomystax, a “fast cycler” twig epiphyte; the thickest part of the branch is 5 mm in diameter; Ecuadorian Amazon. (D) Telipogon sp., a sexually deceptive member of the Oncidiinae; cloud forest near Oxapampa, central Peru. (E) Coryanthes alborosea, pollinated by perfume-seeking male euglossine bees; Peruvian Amazon. (F) Epidendrum atonum, a member of one of the most species-rich orchid genera worldwide; southern Ecuador. (G) Lepanthes pastoensis, representative of the extremely diverse and rapidly evolving subtribe Pleurothallidinae; northern Ecuador. All photographs by Gerardo A. Salazar.

Figure 2

The relationship between specificity for pollinators and species richness of genera. The model represents the Gamma regression and the 95% confidence intervals (shaded area), the results of which are statistically indistinguishable from that of a linear model or LOESS regression. The dataset is from the supporting information of Ackerman et al. [22].

Figure 3

High instability and heterogeneity of the epiphytic habitat makes founding events for epiphytes more frequent, which provides for opportunities for selection and drift. The height of seed release makes long-distance seed dispersal more likely. Pollination systems involving sexual signaling can accelerate the diversification somewhat independently of founder event frequencies for both terrestrials and epiphytes.