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Pollination Mutualism in Insects Before the Evolution of Flowers

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Pollination Mutualism in Insects Before the Evolution of Flowers 5 August 2010 16:9 YB110150.tex McGraw Hill Encyclopedia of Science & Technology, 10th Edition Galley Proofs Keystroked: 25/07/2010 Initial MS Page Sequence Stamp: Article Title: Pollination mutualism in insects before the evolution of flowers Article ID: YB110150 1st Classification Number: 563000 2nd Classification Number: Sequence Number: Pollination mutualism in insects before the evolution of flowers 1 1 2 Pollination mutualism in insects before the 3 evolution of flowers 4 A preeminent association between flowering plants 5 and insects is pollination. Pollination is a mutual- 6 ism in which two interactors reciprocally benefit: 7 a host plant receives the service of insect polli- 8 nation in return for a reward provided for its in- 9 sect pollinator. Typically, the reward is nectar or 10 pollen, but occasionally the provision can be a mat- 11 ing site, resin for nest construction, floral aroma, 12 or even the attraction of plant-generated heat. Evi- 13 dence from the fossil record and from the inferred 14 ecological and phylogenetic relationships between 15 flowering plants (angiosperms) and their insect pol- 16 linators indicates that these types of associations ini- 17 tially were launched during the Early Cretaceous, 18 125–90 million years ago. It was from this interval 19 of time that flowering plants experienced their ini- 20 tial radiation, as did major groups of insects, espe- 21 cially Thysanoptera (thrips), Coleoptera (beetles), 22 Diptera (flies), Lepidoptera (moths and butterflies), 23 and Hymenoptera (sawflies, wasps, ants, and bees). 24 However, until recently, very little was known about 25 more ancient modes of insect pollination, those that 26 predated the appearance of flowering plants or that 27 occurred before angiosperms became dominant in 28 terrestrial ecosystems. 29 Types of evidence. There are several dietary pre- 30 cursors to the consumption of pollen and nectar as 31 a reward for pollination. As far back as the Early 32 Devonian, 416–397 million years ago, small, 33 mandibulate (chewing) arthropods were consum- 34 ing the spores of well-known, early land plants. Ev- 35 idence for this feeding style consists of the sporan- 36 gial contents of single species of host plants found 37 as identifiable spores in coprolites (preserved fecal 38 pellets) that were defecated by small arthropods. 39 Later evidence from the Early Permian, 299–271 mil- 40 lion years ago, includes the prepollen and pollen 41 of seed plants found in the coprolites of insects 42 such as booklice (see illus. a). Of course, pollen 43 consumption by insects is a pattern that contin- 44 ues today. However, it is especially demonstrated 45 by the gut contents extracted from extinct, mid- 46 Mesozoic sawflies (illus. b). These sawflies typically 47 consumed gymnosperm pollen provided by gne- 48 taleans (illus. c), which are represented currently by 49 Ephedra (Mormon tea), Gnetum (a tropical shrub 50 or vine), and Welwitschia (an unusual plant of the 51 southern African Namib Desert). Other extinct lin- 52 eages that provided pollen for insect consumption 53 included seed ferns and, notably, cheirolepidiaceous 54 conifers, whose distinctive pollen has been found 55 as gut contents and clumps plastered to the heads 56 and mouthparts of insects (illus. d). In contrast, flu- 57 ids (such as the nectarlike pollination drops of gym- 58 nosperms) are not preserved in dispersed coprolites 59 or the guts of insects. Thus, insect feeding on flu- 60 ids is inferred by distinctive, siphonlike mouthparts, 61 such as those from extinct species of flies (illus. e) 62 or scorpionflies (illus. f). 5 August 2010 16:9 YB110150.tex Galley Proofs 2 Pollination mutualism in insects before the evolution of flowers 63 Several features of the ovulate and pollen organs of 64 many gymnospermous plants directly implicate the 65 fluid feeding by insects bearing siphonate mouth- 66 parts. These features included elongate tubular mi- 67 cropyles (minute openings in the integument at 68 the tip of an ovule through which the pollen tube 69 commonly enters; illus. g) that occur only in gym- 70 nosperms, deep channels through ovulate-covering 71 tissue that allowed access to pollination-drop re- 72 wards secreted by deep-seated ovules (illus. h), and 73 channels formed by the partial closure of a bivalved 74 ovule, allowing proboscis-bearing insects to imbibe 75 inner pollination drops (illus. i). This varied evi- 76 dence, including coprolites and gut contents from 77 mandibulate insects that fed on pollen grains, the dis- 78 tinctive long-proboscate mouthparts of insects that 79 fed on pollination drops, and plant structures that re- 80 ceived the size-matched proboscises of insects, col- 81 lectively indicates the presence of pollination during 82 the preangiospermous Mesozoic. Evidently, there 83 were two major modes of insect pollination: (1) 84 long-proboscid, fluid-feeding insects that fed on gym- 85 nosperm reproductive organs, in which the reward 86 was principally nectar; and (2) mandibulate, chew- 87 ing insects, whose adults consumed mostly pollen 88 and whose larvae tunneled through vegetative tissue 89 and ovules of plant hosts, including extinct bennet- 90 titaleans and the extant cycads. 91 Major players. The spectrum of mandibulate in- 92 sect pollinators that occurred before the advent 93 of angiosperms, during the Permian, included the 94 Psocoptera (booklice) and Grylloblattodea (rock 95 crawlers), as well as extinct groups related to or- 96 thopteroids (currently, grasshoppers and relatives) 97 and hemipteroids (currently, cicadas, aphids, true 98 bugs, and relatives). After the end-Permian extinc- 99 tion and during the Mesozoic, this spectrum of in- 100 sects was replaced by various lineages of Coleoptera, 101 whose life cycles were associated intimately with 102 bennettitaleans and cycads, and some taxa that be- 103 came affiliated with the large, showy flowers of 104 basal angiosperms (for example, members of the 105 magnolia and laurel families). In contrast, an ar- 106 ray of small, fluid-feeding, long-proboscate insects 107 included early forms of Trichoptera (stem-group 108 caddisflies), Mecoptera (aneuretopsychine scorpi- 109 onflies), and Neuroptera (butterfly-like kalligram- 110 matid lacewings), as well as three or four major 111 lineages of brachyceran Diptera (tanglevein flies, 112 horseflies, and flower-loving flies). With the excep- 113 tion of the brachyceran Diptera, this gymnosperm- 114 pollinating assemblage was replaced, during the di- 115 versification of angiosperms in the Early Cretaceous, 116 by the Lepidoptera (glossate moths), more advanced 117 groups of Diptera (hover flies and bee flies), many 118 lineages of Hymenoptera (wasps and bees), and 119 probably blister beetles with siphonate proboscises. 120 Based on the structure of ovulate and pollen or- 121 gans consistent with a pollinator function, gym- 122 nospermous plant hosts for these lineages were 123 predominantly cycads, bennettitaleans, seed ferns, 124 cheirolepidiaceous conifers, and gnetaleans. Cycads 5 August 2010 16:9 YB110150.tex Galley Proofs Pollination mutualism in insects before the evolution of flowers 3 125 and bennettitaleans typically were composed of 126 fleshy, thick stems that were predominantly beetle- 127 pollinated and involved sacrifice of internal tissues to 128 larvae for completion of their life cycle. Various seed 129 fern groups included caytonialeans, corystosperms, 130 and lepidostrobaleans that bore ovulate organs 131 (illus. g–i), which secreted pollination drops for im- 132 bibation by insects, and produced pollen that may 133 have been consumed as particles by insects with 134 siphons that bore accommodating food tubes. Gne- 135 taleans were considerably more diverse during the 136 Mesozoic and undoubtedly were insect-pollinated, 137 based on a variety of reproductive features, in- 138 cluding pollen consistent with insect vectoring. A 139 plant host with the most distinctive and bizarre 140 type of insect pollination was the cheirolepidiaceous 141 conifer, Alvinia bohemica. This ovulate cone bore a 142 trichome- and nectary-lined funnel that was directed 143 outward and connected by a “pipe” to an inward- 144 placed ovule that secreted a pollination drop. The 145 deep funnel structure was surrounded by various 146 conspicuous appendages that may have served as a 147 lure to small insects or to large insects with elongate 148 mouthpart siphons. 149 Evolutionary biology. The earliest significant evi- 150 dence for insect pollination is from the Permian, 151 even though earlier occurrences extending to the 152 Early Devonian indicate the presence of spore and 153 pollen consumption by mandibulate insects. Per- 154 mian pollination was mediated overwhelmingly by 155 mandibulate insects, although there is some evi- 156 dence for small, caddisfly-like insects with extended 157 proboscises designed for fluid uptake. After the 158 demise of this assemblage at the end-Permian mass 159 extinction, new lineages of both mandibulate chew- 160 ing and long-proboscid fluid-feeding insects origi- 161 nated by the mid-Mesozoic. Although mandibulate 162 beetles were associated predominantly with ben- 163 nettitaleans and cycads, the former hosts became 164 extinct during the Cretaceous, whereas the latter 165 survive today, probably with similar life cycles. A 166 distinctively different evolutionary trajectory was 167 followed by the long-proboscate lineages of scor- 168 pionflies, lacewings, true flies, and others that diver- 169 sified during the Middle Jurassic and experienced 170 an approximately 60-million-year duration as pollina- 171 tors, principally on a variety of seed ferns, cheirole- 172 pidiaceous conifers, and gnetalean hosts. However, 173 this assemblage of gymnosperm pollinators came to 174 a close with the global turnover of gymnosperm to 175 angiosperm floras that commenced during the mid– 176 Early Cretaceous and was mostly completed during 177 the early Late Cretaceous. Their replacements, on 178 angiosperms, are long-proboscid lineages that are fa- 179 miliar to us today: glossate moths, bee flies and hover 180 flies, wasps and bees, and a broad range of other 181 holometabolous insects that independently evolved 182 siphonate mouthparts.
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