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).