Seed germination in cleistogamous species: theoretical considerations and a literature survey of experimental results

Abstract

A cleistogamous species consists of individuals that produce both chasmogamous (open, CH) and cleistogamous (permanently closed, CL) flowers, which facilitates a mixed-mating system. In contrast to what one might expect, CL (obligately selfed) seeds and the plants derived from them can be more fit than CH (potentially outcrossed) seeds and the plants they give rise to. Our aim was to review some theoretical aspects of mixed mating in relation to retention of both CH and CL in cleistogamous species and to determine if data on germination support the notion that CL is advantageous over that of CH. Based on germination (or seedling emergence) of CHvsCL seeds in 29 species in 21 genera and 11 families of monocots and eudicots, CL seeds germinated better in 107 and equally well as in 64 of 252 case studies as CH seeds (67.9%), and the (CH < CL):(CH > CL) ratio was 107/81 (1.32). We conclude that our study lends support to the notion that production of CL seeds by cleistogamous species is advantageous over that of CH seeds. Retention of CH by CL species may be due to the need to prevent complete selfing (s= 1.0) and thus total inbreeding depression (δ), which theory predicts would decrease reproductive success. Some caveats concerning the results of comparative studies on the germination biology of CHvsCL seeds of amphicarpicsensu strictoFabaceae species andCommelina benghalensisand the aerial cleistogamous grassDanthonia spicataare discussed.

Pollen limitation and its effect on seed germination

“…That is, seeds resulting from pollen supplementation, pollen competition and outcrossing may or may not germinate better than those resulting from open pollination (not pollen supplemented), lack of pollen competition and selfing, respectively. Furthermore, seeds from chasmogamous flowers (open, potentially outcrossed) may or may not germinate better than those from cleistogamous flowers (closed, obligately selfed) (Baskin and Baskin, 2017). In general, then, these results seem to suggest that neither amount of pollen (pollen supplementation), quality of pollen (pollen competition) nor outcross vs selfing mating system has a definite influence on germination of the resulting seeds.…”

Amphicarpic plants: definition, ecology, geographic distribution, systematics, life history, evolution and use in agriculture

“…In the amphicarpic sensu stricto species Vigna minima (Gopinathan & Babu, 1987), Amphicarpaea bracteata (Schnee & Waller, 1986; Trapp, 1988) and A. edgeworthii (Zhang et al ., 2015), plants produce subterranean CL flowers and both aerial CL and CH flowers, whereas in the amphicarpic sensu stricto species Amphicarpum amphicarpon (McNamara & Quinn, 1977), Cardamine chenopodifolia (Cheplick, 1983) and Commelina benghalensis (Maheshwari & Maheshwari, 1955) plants produce CL flowers underground and CH flowers aboveground. On the other hand, amphicarpic sensu lato plants of Catananche lutea (Ruiz de Clavijo, 1995), Gymnarrhena micrantha (Koller & Roth, 1964; Plitmann, 1973) and Emex spinosa (Plitmann, 1973; Evenari et al ., 1977) produce potentially outcrossing aerial CH flowers and fruits aboveground and potentially outcrossing aerial (near soil surface) CH flowers that are pulled into the soil shortly after they are insect‐pollinated and thus produce subterranean seeds (see Baskin & Baskin, 2017). In general, aerial CH flowers are large and brightly coloured and subterranean flowers small, white and invariably much reduced, with a small, non‐pigmented corolla enclosed in much‐reduced, scale‐like sepals (Speroni & Izaguirre, 2001, 2003; Zhang, Yang, & Rao, 2006; Kumar et al ., 2012).…”

“…However, CL flowers increase the susceptibility of a population to genetic drift and inbreeding depression if deleterious alleles cannot be purged (Zeide, 1978; Oakley et al ., 2007; see papers on purging by Crnokrak & Barrett, 2002 and Dart & Eckert, 2013). Fitness trade‐offs between CH and CL flowers help maintain amphicarpy as a mixed‐mating strategy (see Baskin & Baskin, 2017 and references cited therein). Furthermore, the genetic variation generated by CH outcrossing could facilitate adaptation of cleistogamous species to environmental change (Oakley et al ., 2007).…”

“…In a recent review paper on seed germination of cleistogamous species, Baskin & Baskin (2017) reported the results of 65 case studies on the germination of aerial (A) versus subterranean (S) seeds for one amphicarpic sensu stricto species of Brassicaceae ( Cardamine chenopodiifolia ), one of Commelinaceae ( Commelina benghalensis ), four of Fabaceae ( Amphicarpaea bracteata , A. edgeworthii , Lathyrus ciliolatus and Vicia sativa var. amphicarpa , all subfamily Papilionoideae) and one of Poaceae ( Amphicarpum amphicarpon ).…”

“…In species that produce both CH and CL, the ratio of CH/CL flowers can also be affected by biotic and abiotic factors such as light level, nutrient availability and herbivory (Fukui & Takahashi, 1975; Culley & Klooster, 2007). Production of CL flowers is often favoured under stressful growth conditions (Cheplick, 1987; Trapp & Hendrix, 1988), apparently because they are energetically less costly to produce than CH flowers (Culley & Klooster, 2007; see Baskin & Baskin, 2017). With an increase in density in A. amphicarpon (as Amphicarpum purshii ), dry mass allocated to CL was remarkably constant, varying from only 13 to 16%.…”