Self-incompatibility limits sexual reproduction rather than environmental conditions in an invasive aquatic plant

Abstract

<jats:title>Summary</jats:title><jats:p><jats:list list-type="order"><jats:list-item><jats:p>Fruitfulness and fertility are important components of sexual reproductive success in plants, and often depends on environmental conditions and reproductive systems. For invasive plants, fruitfulness and fertility control their ecological success and adaptation in invaded ecosystems. We studied which factors bring about fruitfulness and fertility in invasive populations of the aquatic plant <jats:italic>Ludwigia grandiflora</jats:italic> subsp. <jats:italic>hexapetala</jats:italic>.</jats:p></jats:list-item><jats:list-item><jats:p>We analysed fruitfulness and fertility of 37 populations growing under variable climatic conditions in Western Europe, and sub-sampled fruitful and fruitless populations grown in common controlled conditions. We carried out self- and cross-pollinations and measured their floral biometrics.</jats:p></jats:list-item><jats:list-item><jats:p>Environmental conditions, and temperature in particular, did not affect fruitfulness and fertility in-situ or in common controlled environments. Hand-pollinations resulted in fruit production by individuals sampled from fruitless populations when pollen came from fruitful populations, and by individuals sampled from fruitful populations whatever the origin of pollen. Floral biometrics evidenced the existence of two floral morphs that overlapped with fruitfulness, and individual incompatibility.</jats:p></jats:list-item><jats:list-item><jats:p>Our results rebutted the hypothesis that environmental conditions control fruitfulness and fertility in these invasive populations. We instead found that fruit and seed production were controlled by a reproductive system involving a self-incompatible approach herkogamous morph and a self-compatible reverse herkogamous morph. We assessed the floral morphs distribution worldwide of fruitless and fruitful native and invasive populations that matched our results at larger scale. Our results may constitute the first evidence of a possible heteromorphic self-incompatible system in <jats:italic>Ludwigia</jats:italic> populations and in Onagraceae phylogeny. It calls for further investigations on reproductive systems in this plant family. Finally, the observation that the self-incompatible morph seemed to be the world most invasive morph in this species tackles our understanding of biological and ecological conditions for invasiveness.</jats:p></jats:list-item><jats:list-item><jats:p><jats:italic>Synthesis</jats:italic>. Our study showed that fruitfulness and fertility in the aquatic invasive plant, <jats:italic>Ludwigia grandiflora</jats:italic> subsp. <jats:italic>hexapetala</jats:italic> depend on a self-incompatibility system coinciding with two floral morphs, rather than environmental conditions and limitations. These new explanations on the sexual success of <jats:italic>Ludwigia</jats:italic> invasive populations will help defining new predictions about its worldwide spreads and ecological success, and will help reappraising future management plans.</jats:p></jats:list-item></jats:list></jats:p>

Reproductive modes in populations of late-acting self-incompatible and self-compatible polyploidLudwigia grandiflorasubsp.hexapetalain western Europe

“…In SC populations of Lgh (S-morph), pollen tubes of the L-morph (LSI type) grow significantly faster in SC individuals (Portillo-Lemus et al 2022). It seems a sufficient and efficient mechanism to favour outcrossing when compatible pollens are available in western European…”

“…On its side, Lgh presents heteromorphic flowers corresponding to two floral morphs: L-morph individuals develop long-styled flowers and S-morph individuals develop short-styled flowers (Portillo-Lemus et al 2021). L-morph flowers express an active LSI in western European populations (Portillo-Lemus et al 2022). During the core flowering season (summer), in experimental greenhouse conditions, L-morph individuals show a stable seemingly insignificant rate of autogamy (around 0.2‰ of the available ovules) that increases at the end of the flowering season, during autumn, to 1‰, which is common in LSI systems (Gibbs 2014.…”

“…This pattern of low rates of autogamy, that increase at the end of the flowering season, may provide the advantage of reproductive assurance (Goodwillie & Weber 2018). In contrast, S-morph individuals are self-compatible (SC) in western European populations but pollen tubes of the L-morph grow significantly faster and are thus advantaged to fertilize ovules when in competition with self-pollen (Portillo-Lemus et al 2022). In addition, peripatric Lgh populations, including European populations, were previously reported as exclusively clonal with few clonal lines (Dandelot 2004, Okada et al 2009.…”