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. 2024 May 24;15(1):4392.
doi: 10.1038/s41467-024-48646-x.

Convergent evolution of fern nectaries facilitated independent recruitment of ant-bodyguards from flowering plants

Jacob S Suissa  1 , Fay-Wei Li  2   3 , Corrie S Moreau  4   5
Affiliations

Convergent evolution of fern nectaries facilitated independent recruitment of ant-bodyguards from flowering plants

Jacob S Suissa et al. Nat Commun. .

Abstract

Plant-herbivore interactions reciprocally influence species' evolutionary trajectories. These interactions have led to many physical and chemical defenses across the plant kingdom. Some plants have even evolved indirect defense strategies to outsource their protection to ant bodyguards by bribing them with a sugary reward (nectar). Identifying the evolutionary processes underpinning these indirect defenses provide insight into the evolution of plant-animal interactions. Using a cross-kingdom, phylogenetic approach, we examined the convergent evolution of ant-guarding nectaries across ferns and flowering plants. Here, we discover that nectaries originated in ferns and flowering plants concurrently during the Cretaceous, coinciding with the rise of plant associations in ants. While nectaries in flowering plants evolved steadily through time, ferns showed a pronounced lag of nearly 100 My between their origin and subsequent diversification in the Cenozoic. Importantly, we find that as ferns transitioned from the forest floor into the canopy, they secondarily recruited ant bodyguards from existing ant-angiosperm relationships.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Diversity of fern nectaries.
a gland-tipped nectar-secreting trichomes of Lygodium microphyllum. b raised nectar gland of Gymnosphaera henryi. c raised pigmented nectar gland of Pteridium aquilinum d microscopic adaxial nectar pore of Pleopeltis thysannolepis. e microscopic abaxial nectar pore of Drynaria pilosa. f cup-like nectary of Drynaria speciosa. Photographs from JSS, except G. henryi which was provided with permission by Shiyong Dong.
Fig. 2
Fig. 2. Ancestral character estimation of nectary evolution in ferns.
Genera that lacked nectaries were pruned to 1 tip per genus. Ancestral character estimation suggests that nectaries had the potential to evolve in the Cretaceous. However, while nectaries likely had a deep origin, many of the lineages with nectaries did not diversify until the Cenozoic. Ancestral character estimation was implemented using stochastic character mapping. Pie charts at nodes along the time-calibrated fern phylogeny represent ancestral states calculated as the marginal posterior probability of nectary presence (green) or unobserved (gray). Colors along the branches represent estimated character states summarized across 100 randomly selected posterior samples of character histories from 1000 stochastic character maps. Bars at tips indicate the species character state for nectary presence or absence. Bars along the perimeter of the reconstructed tree and bolded letters indicate major fern clades. Light pink: Aspleniineae, Green Polypodiineae, Brown: Pteridineae, Red: Equisetales, Dark orange: Ophioglossales & Psilotales, Teal: Marattiales, Blue: Hymenophyllales, Yellow: Gleicheniales, Cream: Schizaeales, Black: Salviniales, Purple: Cyatheales, Light blue Lindsaeineae, Pink: Dennstaedtiineae. Black inlaid circles indicate 100-million-year time intervals. Photo inset of an ant feeding on fern nectar taken by JSS.
Fig. 3
Fig. 3. Distribution of timing around nectary origin in ferns (green), EFNs in flowering plants (blue), and plant associations in ants (red), derived from 100 stochastic character maps.
Boxplot inset depicts a set of unpaired two-sided Wilcox tests between the timing of each trait with a Bonferroni correction. The center line within each box denotes the median value, while the bounds of the box represent the interquartile range (IQR), encapsulating the middle 50% of the data, the lower portion of the box represents the 25th percentile, while the upper portion of the box denotes the 75th percentile. The whiskers extend from the box to the minima and maxima, respectively. The timing of nectary origin and ferns and flowering plants is not significantly different, while ant-plant associations seemed to have evolved slightly later. P-value for each pairwise comparison is as follows: Ferns:Angiosperms (p = 0.35), Ferns:Ants (p < 2.22e−16), Angiosperms:Ants (p < 2.22e−16).
Fig. 4
Fig. 4. Cross-kingdom lineage-through time plot.
Nectaries across ferns, EFNs in flowering plants, and ants associated with plants likely originated around the middle Cretaceous. However, an almost 100-million-year lag in the diversification of ferns with nectaries may relate to the rise of fern insect herbivores in the Cenozoic (however, we have limited support for this hypothesis). Lineage-through-time (LTT) plots from 100 stochastic character maps for ferns with nectaries, angiosperms with extrafloral nectaries, and ants associated with plants. Each line represents a single LTT plot for 1/100 stochastic character maps, the thicker central lines represent the average LTT across all maps. Fern herbivore LTT plot is derived from a singular tree given the data used. The LTT plot shows the cumulative number of lineages through time for each group, as indicated by the colored lines on the graph. The x-axis represents time in millions of years before the present (mya). Inlaid in the plot is a stochastic character map indicating the ancestral state reconstruction of the presence or absence of fern nectaries (for more detail see Fig. 2). Black lines are fern lineages hypothesized to possess nectaries and those in gray are lineages unobserved nectaries. Photo inset of ants feeding on Bracken fern nectaries taken by JSS.
Fig. 5
Fig. 5. Evolution of nectaries in ferns facilitated by shifts from understory to canopy-dwelling habitat.
a Summary of 50 sampled stochastic character maps showing the transitions and correlated evolution between growth habit and nectary presence (colors indicating dual states shown in the inset in the bottom left of plate a). Ancestral character estimation was implemented using stochastic character mapping. Pie charts at nodes along the time-calibrated fern phylogeny represent ancestral states calculated as the marginal posterior probability of nectary presence and growth habit. Blue: nectary not observed understory, Green: nectary not observed canopy-dwelling, Yellow: nectary observed canopy-dwelling, Brown: nectary observed understory. Colors along the branches represent estimated character states summarized across 50 randomly selected posterior samples of character histories from 100 stochastic character maps. Bars at the tips indicate the species character state for the dual trait. b Distribution of fern species with nectaries and their growth habit. Top: Proportion of total nectary-bearing species in each growth habit. Of the 149 fern species bearing nectaries most were tree ferns (Arb: 50.3%), then epiphytic (Epi: 43.0%) and climbing (Climb: 4.0%), with the fewest species being understory (Terr: 2.7%). Bottom: Proportion of total fern species in each growth habit-bearing nectaries. Nectary-bearing species are disproportionately enriched in canopy-dwelling species (Arb: 15.33%), (Epi: 6.90%), (Clim: 7.6%), (Ter: 0.19%). c Phylogeny with red highlighted branches depicting which parts of the phylogeny are in Rate 1 (red) or Rate 2 (blue). Colors along the branches represent estimated rate category summarized across 50 randomly selected posterior samples from the stochastic character maps. d Best-fitting model from CorHMM depicting the transition rates between dual characters. Rates are individual changes per million years. Colors of arrows related to the speed of transition (cool being lower and hot being faster). Transition between rate categories denoted by large blue arrow in between both matrixes. Bars along the perimeter of the reconstructed trees and bolded letters indicate major fern clades. As: Aspleniineae, Po: Polypodiineae, Pt: Pteridineae, Eq: Equisetales, OP: Ophioglossales & Psilotales, Ma: Marattiales, Hy: Hymenophyllales, Gl: Gleicheniales, Sc: Schizaeales, Sa: Salviniales, Cy: Cyatheales, De: Dennstaedtiineae. Canopy-dwelling indicates elevated leaves (i.e., Tre: tree ferns, Epi: epiphytic, Clim: climbing). Understory, non-canopy-dwelling species denoted as Ter (terrestrial).
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