On the selective advantage of coloniality in staghorn ferns (Platycerium bifurcatum, Polypodiaceae)

ABSTRACT

The staghorn fern (Platycerium bifurcatum, Polypodiaceae) is an epiphyte from Australasia that displays many life history characteristics commonly associated with eusocial animals. Here, I hypothesize about the selective advantage of living in cooperative groups by comparing the morphological characteristics of colonies to their solitary congeners.

KEYWORDS:

• Biological complexity
• Epiphyte
• Eusociality

Life on earth is remarkably complex. Yet it began very differently, from simple, self-replicating molecules. The evolution of increasing biological complexity, from simple molecules to sophisticated societies, is one of the deepest enigmas in our understanding of life on earth.

Biological complexity arises from ‘major evolutionary transitions’, which occur when independent entities begin to cooperate, resulting in a new, more complex lifeform.¹ Notable examples of major transitions include the evolution of eukaryotic cells from archaea and eubacteria, the evolution of multicellular organisms from single-celled ancestors, and the evolution of eusocial colonies from solitary individuals.²

Despite its importance to our understanding of biological complexity, eusociality is known only in a few types of animals. Until recently, it has not been observed in plants, suggesting that plants might be inherently less complex than animals. However, recent research on a colonial, epiphytic fern from Australasia challenges the notion that the door to eusociality is open only to animals.

Without access to soil on the forest floor below, epiphytic plants are regularly subject to water and nutrient stress.³ The staghorn fern (Platycerium bifurcatum, Polypodiaceae) appears to have solved this problem by evolving life history characteristics that are commonly associated with eusocial animals.⁴ More specifically, when growing epiphytically, staghorn ferns always grow in colonies. Plants within colonies differ markedly in morphology and seem to be specialized to perform different tasks. Together they appear to subdivide labor to create a communal store of water and nutrients. Furthermore, just under half of all colony members forgo reproduction. While 4,demonstrate that these life history characteristics are broadly consistent with the three genera criteria delineating eusocial species from solitary species,² they do not identify the selective advantage of being colonial. Here, I try to bridge this gap by developing a hypothesis to explain the evolution of cooperative group living in Platycerium ferns.

The genus Platycerium contains approximately 15 taxa,⁵ most of which are solitary.^6,7 The genus is strongly heterophyllous and all plants produce two types of fronds: (1) ‘strap’ fronds are long, narrow and long-lived, and (2) ‘nest’ fronds are more circular in shape, short-lived and are retained on parent plants long after they senesce. Not only do they differ markedly from each other, but strap and nest fronds can also vary markedly among species. Some species produce circular-shaped nest fronds that clasp the branches of host trees, while in other species they are larger, more erect and fan shaped. Strap fronds vary from stiff and erect, to flexible and pendulant (Figure 1).

Figure 1. Growth form diversity in Platycerium ferns. (a) P. superbum displaying Type I morphology: fan-shaped nest fronds that collect rainwater and pendulant strap fronds that reduce biomechanical demands on root systems (photo credit: Tatiana Gerus). (b) P. ridleyi displaying Type II morphology: clasping nest fronds that promote structural support and water storage, and erect strap fronds that collect rainwater (photo credit: Ganges Lim). (c) P. bifurcatum, a colonial species that exhibits components of both growth forms (photo credit: Ian Hutton). Individuals at the top of colonies produce fan-shaped nest fronds and erect strap fronds, both of which appear adapted to collect rainwater. Individuals at the bottom produce both clasping nest fronds and pendulant strap fronds, which appear to promote structural support. Therefore, colonial living appears to promote several unique combinations of frond forms that are not observed in solitary species

The diversity of frond morphology displayed by solitary Platycerium species can be consolidated into two general growth forms, each of which appears to be adapted to mediate water stress differently. ‘Type I’ solitary species have large, fan-shaped nest fronds that collect water and flexible strap fronds that undergo photosynthesis and reproduction. Strap fronds in this growth form also tend to droop downwards (i.e. pendulously), a common feature in epiphytes that lessons biomechanical demands on root systems (Figure 1a)³. ‘Type II’ solitary species have rounded nest fronds that clasp the branches of host trees for structural support. They also produce stiff, erect, gutter-like strap fronds that collect and channel rainwater down to nest fronds, which also store water (Figure 1b).

While solitary species can generally be classified as having either Type I or Type II morphology, P. bifurcatum colonies defy classification (Figure 1c). Plants at the top of colonies produce a combination of strap and nest frond morphology not seen in solitary species – fan-shaped nest fronds characteristic of Type I solitary species, and erect, gutter-like strap fronds characteristic of Type II solitary species [see ⁴,and Figure 2 for quantitative comparisons]. As a result, both frond types produced by plants at the top of colonies seem to be specialized to collect water. On the other hand, plants at the bottom of colonies produce clasping, circular-shaped nest fronds typical of Type II solitary species, and flexible, pendulant fronds typical of Type I species. Plants at the bottom of colonies thereby appear to be adapted to promote structural support.

Figure 2. Changes in frond angles within a Platycerium bifurcatum colony. The angle of strap fronds was measured on the youngest, fully mature strap frond from 19 individuals within a single colony growing in the glasshouse in the Wellington Botanical Garden. Frond angles, which ranged from 0° when pointed downwards to 180° when pointed upwards (y-axis), increased with their height above the base of the colony (x-axis). Best fit line from linear regression is shown along with the 95% confidence interval (n = 19, t = 7.513, p < .001). Vertically orientated fronds positioned at the tops of colonies may facilitated water capture and transport to individuals below [c.f. ⁸]

Differences in the functional morphology of solitary and colonial staghorn ferns suggest that the evolution of colonial living may be linked to specialization. In solitary species, specialization results from morphological differentiation of organs (i.e. fronds) within plants. However, in P. bifurcatum colonies, specialization results not only from morphological differentiation between fronds within individual plants, but also from differences in frond combinations between plants, which facilitate a greater degree of task specialization than solitary species. Similar patterns in the division of labor have been observed in animal societies^9,10, hinting that a common set of life history circumstances might favor the evolution of colonial living in both plants and animals.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This work was supported by the Royal Society of New Zealand Marsden Fund - MFP - VUW2003.