Evolutionary seed ecology of heteromorphic Amaranthaceae

Seed and fruit structures are one of the key innovations that allow plants to successfully occupy habitats all around the globe, ensuring dispersal, survival of unfavourable conditions and seedling establishment. While adaptive tracking in the majority of plants resulted in a single most optimal seed and fruit phenotype, some plants produce two or more types of morphologically distinct fruits and/or seeds that differ in their ecological and physiological characteristics. These carpological heteromorphisms are a type of bet-hedging strategy and are believed to have developed as a response to an unpredictable spatiotemporally-changing environment. Although recognized already by Charles Darwin, the true extent of this evolutionary phenomenon, its trade-off characteristics, heritability, evolvability, and its environmental and genetic regulation are still insufficiently investigated. Carpological heteromorphisms have been described from several plant families, however, they are most commonly found in Asteraceae and Amaranthaceae sensu lato (including Chenopodiaceae). The latter is an integral part of vegetation occurring in seasonally highly unpredictable semi-arid and arid zones worldwide. Carpological heteromorphisms in this family are multifold and span from morphologically distinct diaspores with different dispersal potentials and fleshy and non-fleshy fruits with different dispersal agents, to morphologically (in)distinct seeds with different germination behaviours. Heterocarpic and heterospermic taxa in Amaranthaceae sensu lato are predominantly diploid, possess relatively small genomes and have a high number of available genomic resources, which could expedite genomic investigations of these carpological heteromorphisms. Nevertheless, knowledge of the evolutionary seed ecology of Amaranthaceae sensu lato is scarce and disconnected. Here we review the literature on ecological, physiological and (epi)genetic aspects of germination and stress tolerance in early ontogenetic stages of heteromorphic Amaranthaceae sensu lato. Furthermore, we critically address the shortcomings of current studies and provide guidelines for further research. The authors anticipate this review to raise interest in this plant family and this biological phenomenon, which harbours a great potential to answer some very fundamental biological questions on how individual angiosperm lineages managed to conquer the most inhospitable habitats worldwide.