Figure 1. Illustration of typical cycad traits and key morphological structures highlighted in the review. Center: Cycas panzhihuaensis habit. a. Push-pull pollination between pollen (left) and ovulate (right) cones. b. Flagellated sperm of Zamia integrifolia , scale = 40 µm. c. Pollen cone with microsporangia bearing pollen grains. d. Ovulate cones with ovules, and seeds after fertilization, example from Zamia neurophyllidia (left) andC. panzhihuaensis (right). Cycas is the only genus to have the loose open ovulate cone. e. Herbivorous Eumaeus atala larvae feeding on a Zamia showing bright red aposematic coloring. f. Leaf with microbiota symbionts of the only epiphytic gymnosperm,Zamia pseudoparasitica, scale = 25 cm. Zamia nana g. Precoralloid roots prior to bacterial infection and h. Coralloid roots, note the blue-green cyanobacterial zone. g. scale = 5 mm, and h. scale = 1 mm. Image b. is reproduced from The Biology of the Cycads,Norstog & Nicholls 1997 Cornell University Press. Central image and image d. are modified from Liu et al . (2022).
Cycad biology
Cycads are one of the largest extant gymnosperm lineages, comprising ten genera and ca. 375 species, two-thirds of which are included on the International Union for Conservation of Nature (IUCN) Red List of threatened species (Calonje et al. , 2023). Cycads are placed at the base of the gymnosperm phylogeny and are amongst the most ancient extant seed plants, with likely origins in the Carboniferous. The biogeography of fossil cycad taxa has shown that cycads were globally widespread in the Jurassic, Cretaceous and early Paloegene, with taxa found in the Arctic and Europe where no extant species occur (Coiroet al. , 2023; Fig. 2). They appear to have undergone a period of extinction with recent radiation in the last ~20 Mya (Nagalingum et al. , 2011; Condamine et al. , 2015; Liuet al. , 2022). Cycads are currently globally distributed in the tropics and subtropics, where they hold considerable cultural significance with a rich history of anthropological and ethnobotanical research (eg. Carrasco et al. , 2022).
Cycads exhibit a striking amount of mutualism in their associations with insects. Entire lineages of both herbivores and pollinators are specialized on cycads, in what has been suggested to be classic examples of coevolution (Tang et al. , 2020; Whitaker & Salzman, 2020). All of these insects must contend with a host of cycad secondary metabolites, some of which are rather rare in the known biological world, and many of the specialist insects are aposematically colored. (Whitaker & Salzman 2020). These dioecious gymnosperms appear to rely almost exclusively on insect vectors for pollination which they maneuver between cone sexes through a series of physiological events that includes cone thermogenesis (Terry et al. , 2016). The brood-site pollination mutualists live their entire life cycles within the reproductive structures of their host cycad, feeding, breeding and laying eggs within the tissue (Terry et al. 2012).
Cycads also engage in symbiosis with microbiota. The plants produce morphologically distinct coralloid roots (Fig. 1h) that house fungi, nitrogen-fixing cyanobacteria and associated bacteria, the functions of which are only recently being elucidated. More recent research suggests that leaf microbial associates may also contribute to plant growth success and habitat diversity, including nitrogen fixation in the world’s only epiphytic gymnosperm species (Zamia pseudoparasitica : Bell-Doyon et al., 2020).
Position in land plant phylogeny
Cycads hold a pivotal position in understanding the origin and evolution of seed plants (Liu et al. , 2022; Coiro et al. , 2023), yet their relationship to other gymnosperms remains unresolved. Extant gymnosperms consist of five major lineages: cycads, Ginkgo , Pinaceae, cupressophytes, and gnetophytes. Although the monophyly of each group is well resolved, the relationships among the five lineages have long been controversial (Xi, Rest & Davis, 2013). As it currently stands, nuclear and plastid genomic data are congruent on a cycad andGinkgo clade as sister to the rest of gymnosperms (Stull et al. , 2021; Liu et al. , 2022). However mitochondrial genomic data support cycads alone being sister to all other gymnosperms (Liu et al ., 2022). Recent advances in cycad genomics (see section VII) places a clearer understanding of seed plant evolutionary history within our grasp.
Generic relationships within the order Cycadales are less controversial with universal consensus on branching order (Fig. 2, Nagalingum et al ., 2011; Condamine et al ., 2015; Liu et al ., 2022). The two extant families, Cycadaceae and Zamiaceae form sister clades. Most cycad diversity is found in Cycas (119 species) and Zamia(86 species) with rather disjunct non-overlapping distributions (Fig. 2). Divergence time estimates, using a total evidence approach including 60 fossil cycads, date the origin of Cycadales back to the Carboniferous (median 330 Mya, 296-358 Mya) (Coiro et al ., 2023), a much older date than other landmark studies focused solely on extant taxa (Nagalingum et al ., 2011; Condamine et al ., 2015; Fig. 2).
While the lineage itself is ancient, most extant genera seem to have diversified in the last ~27 million years in a nearly synchronous fashion (Fig. 2; Calonje et al ., 2019; Nagalingumet al ., 2011). Long stem branches may represent either high extinction or low divergence during the origin of a clade; here the large number of cycad fossils seems to suggest high extinction (Nagalingum et al ., 2011). Phylogenetic analysis using organellar loci has not been efficient in resolving such recent radiations at the species level (Calonje et al ., 2019), initiating a shift to large molecular data sets generated from transcriptome data that provide a clearer understanding of divergence and diversification (Habib et al., 2022; 2023). For example, the most morphologically and ecologically diverse genus, Zamia , has been found to have diversified since the Miocene (~16-24 mya, Calonjeet al ., 2019) with several clades showing a rather surprising biogeographical pattern in the American continent (Calonje et al ., 2019; Lindstrom et al ., in review). In addition, diversifications have not been completely tracked by all loci with several cases of incomplete lineage sorting and phylogenomic incongruence in several key nodes in Macrozamia ,Ceratozamia and Zamia (Habib et al ., 2022; 2023; Lindstrom et al ., in review). As in many plant studies, ancient and recent reticulation are widespread in all genera, ideal for further intraspecific studies using the wealth of genomic data available as recently done in species of the genus Dioon (Gutiérrez-Ortegaet al ., 2020), Ceratozamia (Gutiérrez-Ortega et al ., 2023); Cycas (He et al ., 2023) and Zamiausing microsatellites (Salas-Leiva et al ., 2017 and references therein).