Long-term morphological stasis maintained by a plant–pollinator mutualism

Davis, Charles C.; Schaefer, Hanno; Xi, Zhenxiang; Baum, David A.; Donoghue, Michael J.; Harmon, Luke J.

doi:10.1073/pnas.1403157111

Cited by 90 publications

(108 citation statements)

References 71 publications

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“…Morphological evolution can accelerate when selection on a trait is removed and the body plan is free to change if developmental constraints are limited (56,57), or it can slow down when ecological opportunity diminishes simultaneously (58). Here we showed that mutualistic strategy profoundly affects the pace of morphological change in traits involved in the interaction.…”

Section: Relaxed Selective Constraints On Entrance Diameter After Mutmentioning

confidence: 62%

Partner abundance controls mutualism stability and the pace of morphological change over geologic time

Chomicki

Renner

2017

Proc. Natl. Acad. Sci. U.S.A.

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Mutualisms that involve symbioses among specialized partners may be more stable than mutualisms among generalists, and theoretical models predict that in many mutualisms, partners exert reciprocal stabilizing selection on traits directly involved in the interaction. A corollary is that mutualism breakdown should increase morphological rates of evolution. We here use the largest ant-plant clade (Hydnophytinae), with different levels of specialization for mutualistic ant symbionts, to study the ecological context of mutualism breakdown and the response of a key symbiosis-related trait, domatium entrance hole size, which filters symbionts by size. Our analyses support three predictions from mutualism theory. First, all 12 losses apparently only occur from a generalist symbiotic state. Second, mutualism losses occurred where symbionts are scarce, in our system at high altitudes. Third, domatium entrance hole size barely changes in specialized symbiotic species, but evolves rapidly once symbiosis with ants has broken down, with a "morphorate map" revealing that hotspots of entrance hole evolution are clustered in high-altitude areas. Our study reveals that mutualistic strategy profoundly affects the pace of morphological change in traits involved in the interaction and suggests that shifts in partners' relative abundances may frequently drive reversions of generalist mutualisms to autonomy. mutualism | symbiosis | morphology | comparative phylogenetic methods | ants U nderstanding how mutualisms arise, persist, or break down is a major focus in ecology and evolutionary biology (1-3). Symbiotic mutualisms can revert to the free-living state if the costto-benefit ratio shifts so that costs outweigh benefits. There are three main pathways through which mutualism can break down, namely, extinction of the partner, reversion to the free-living state, or shift to parasitism (2). Extinction of one partner in an obligate mutualism should entail the extinction of the other, whereas in a facultative mutualism, extinction might lead to a reversion to autonomy (4-8), but these predictions have limited support from empirical studies. Similarly, mutualism could also break down if one partner becomes scarce, which may be especially important in laterally transferred symbioses where partners disperse independently and the interaction needs to be reestablished at each generation, involving vulnerable stages for both. Mutualisms can also break down by shifting to parasitism. Such shifts are predicted by theory (9, 10) because reducing or stopping reciprocation increases the fitness of the cheating partner (11)(12)(13)(14). Phylogenetically unrelated freeloaders may also disrupt a mutualism by exploiting it (15-18). Finally, mutualism can break down if benefits can be obtained cheaply or freely from the environment, for example, when plants involved in mycorrhizal or rhizobia symbioses grow in nutrient-rich soils (19,20) or when antiherbivore defense by ant mutualists is no longer required (21). Most of these theoretical expectations ab...

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Section: Relaxed Selective Constraints On Entrance Diameter After Mutmentioning

confidence: 62%

Partner abundance controls mutualism stability and the pace of morphological change over geologic time

Chomicki

Renner

2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Such inference can be made for the genus Banisteriopsis, as demonstrated by our data. Interestingly, selection for plant-pollinator mutualism (extrinsic factors) has been used to explain the origin and conserved floral morphology of Malpighiaceae (Davis et al 2014). Such hypothesis is based on clades that have lost interaction oil-bee pollination display major evolutionary shifts in floral characters related with this interaction (Davis et al 2014).…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, selection for plant-pollinator mutualism (extrinsic factors) has been used to explain the origin and conserved floral morphology of Malpighiaceae (Davis et al 2014). Such hypothesis is based on clades that have lost interaction oil-bee pollination display major evolutionary shifts in floral characters related with this interaction (Davis et al 2014). The presence of protein granules in the calyx glands of Banisteriopsis may be related to the energetic demands of pollinators, as proposed by Nicolson & Thornburg (2007) who considered amino acids as an important resource for visitors.…”

Section: Discussionmentioning

confidence: 99%

“…In the same way, Durkee et al (1984) suggested that the EFNs of Passiflora foetida represent a transition to lipid-secreting glands. In additional, Davis et al (2014) consider the conserved floral morphology in Malpighiaceae as a result of extrinsic factor, in especially the plant-pollinator mutualism. The complexity of secretions produced by the leaf glands of the species studied here shows that the metabolism of these glands can be altered, which provides additional evidence of the importance of plant-animal interactions in the diversification of Malpighiaceae.…”

Section: Discussionmentioning

confidence: 99%

“…When stamens or styles are heteromorphic they tend to remain symmetrical with respect to this front-toback axis (Niedenzu 1928;Anderson 1977;1979;. The hypothesis for the conservation of floral morphology within the Malpighiaceae for tens of millions of years of evolution is based on the selection imposed by their specialist New World oil-bee pollinators (Davis et al 2014).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Comparative anatomy of calyx and foliar glands of Banisteriopsis C. B. Rob. (Malpighiaceae)

Araújo

Meira

2016

Acta Bot. Bras.

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Banisteriopsis is considered one of the largest genera of Malpighiaceae with 58 species, of which 47 occur in Brazil. The typical calyx and leaf glands of Banisteriopsis are considered relevant to the adaptive success of Malpighiaceae. Comparative studies of anatomical and histochemical characteristics may reveal similarities and assist in the interpretation of the functions performed by such glands. The present study aimed to describe the anatomy of the calyx and leaf glands of 38 species of Banisteriopsis that occur in Brazil, and to analyze these structures histochemically in B. campestris, B. laevifolia and B malifolia, using standard methods. Calyx glands differ from leaf glands by possessing an irregular surface that is covered by a thick cuticle that is released from the epidermis by the accumulation of secretion; the glands are similar in all the other anatomical characteristics. Both types of glands produce secretions composed of a mixture of protein granules, lipids and polysaccharides. These findings reinforce the hypothesis that foliar glands have given rise to calyx glands in response to interactions with pollinators.

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First report of laticifers in lianas of Malpighiaceae and their phylogenetic implications

Pace

Neto

Santos‐Silva

et al. 2019

American J of Botany

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PremiseLaticifers have evolved multiple times in angiosperms and have been interpreted as a key innovation involved in plant defense mechanisms. In Malpighiaceae, laticifers were previously known from a single lineage of trees and shrubs, the Galphimia clade, but with detailed anatomical analyses here, we show that their distribution is broader in the family, also encompassing large clades of lianas.MethodsFrom 15 genera, 70 species of Malpighiaceae were surveyed through careful anatomical ontogenetic analysis of roots, stems, and leaves and detailed histochemical tests to elucidate the nature of laticifers and latex in the family.ResultsArticulated anastomosing laticifers were encountered in roots, stems, and leaves of two distantly related megadiverse genera of Malpighiaceae lianas: Stigmaphyllon (stigmaphylloid clade) and Tetrapterys s.s. (tetrapteroid clade). From the apex downward, in Stigmaphyllon the laticifers are derived from the procambium and from the cambium during its early activity and are present in the outermost part of the vascular cylinder of stems and leaves and in the pericycle of roots, whereas in Tetrapterys s.s. they are derived from the ground meristem, procambium, and cambium throughout the plant body and are present in the cortex and pith, either the pericycle in roots or the outermost part of the vascular system in stems and leaves, and the primary and secondary phloem.ConclusionsLaticifers seem to have evolved at least three times independently in Malpighiaceae, once in a lineage of trees and shrubs and twice in two distantly related megadiverse lianescent lineages. Laticifer evolution in Malpighiaceae is homoplastic and may be related to increases in species diversification.

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Long-term morphological stasis maintained by a plant–pollinator mutualism

Cited by 90 publications

References 71 publications

Partner abundance controls mutualism stability and the pace of morphological change over geologic time

Partner abundance controls mutualism stability and the pace of morphological change over geologic time

Comparative anatomy of calyx and foliar glands of Banisteriopsis C. B. Rob. (Malpighiaceae)

First report of laticifers in lianas of Malpighiaceae and their phylogenetic implications

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