6 NOVEMBER 2009 VOL 326 SCIENCE www.sciencemag.org 808 PERSPECTIVES Evolution of Animal Pollination PALEONTOLOGY Jeff Ollerton and Emma Coulthard Animals pollinated specialized seed plants even before flowering plants evolved. T he evolution of animal pollination in flowering plants (angiosperms) and the resulting coevolution and diver- sification of both angiosperms and major pollinator groups during the late Cretaceous (99.6 to 65.5 million years ago) is one of the classic stories of evolutionary biology ( 1). On page 840 of this issue, however, Ren et al. ( 2) challenge aspects of this story and hint at a much more complex ecological scenario for the evolution of plant-pollina- tor relationships. An important feature of the traditional story is that the non-angiosperm seed plants living during the Mesozoic (251 to 65.5 mil- lion years ago) were mainly wind-pollinated. Although the fossil record of these plants shows evidence of possible animal pollina- tion as early as the late Carboniferous (320 to 300 million years ago) ( 3), this evidence is open to interpretations of the size of pol- len grains (apparently too large to be wind- dispersed), the possibly attractive function of reproductive organs, and patterns of damage by insects. The assumption is that although animal pollination may predate the evolution of the flowering plants, it was rare and unspe- cialized relative to what was to follow in the late Cretaceous ( 4). Ren et al. now marshal evidence from an impressive range of sources—from compara- tive morphology of fossil insect mouthparts to elemental analysis of the fossils and their surrounding matrix—to propose that a previ- ously overlooked group of Mesozoic scorpi- onflies was able to feed on a nectarlike fluid ( 5) produced by a group of now-extinct non- angiosperm seed plants. The authors suggest that the scorpionflies in turn pollinated the plants. This may be the earliest known exam- ple of coevolution between plants and polli- nators. The evidence that Ren et al. present is compelling, and if they are correct, it will change our understanding of the early ecol- ogy and evolution of pollination by insects. As Darwin ( 6) famously recognized when he speculated about the coevolution of flower and tongue length between the Madagascan orchid Angraecum sesquipedale and its (then unknown) moth pollinator, flowering plants have often evolved tubular structures that hold nectar or protect reproductive organs. The plants can thus discriminate between flower visitors, enabling them to specialize on pollinators with appropriately sized mouth- parts ( 7, 8). This match between mouthparts and flower depth ( 9) facilitates more accurate pollen placement, meaning that less pollen is wasted, and prevents nonpollinating animals from robbing nectar. It may be a major fac- tor driving the diversification of some angio- sperm genera ( 8) and structuring the patterns of interaction with pollinators in plant com- munities ( 10), but until Ren et al.’s study, it was considered unimportant in non-angio- sperm pollination. The 11 scorpionfly species described by Ren et al. have mouthparts that are both rela- tively long and consistent with fluid feeding by sucking. The species represent three dif- ferent families, pointing to repeated conver- gent evolution of this feeding strategy, which in turn suggests that substantial quantities of nectarlike fluid ( 5) were available to these taxa. Ren et al. believe that the source was a group of non-angiosperm seed plants belong- ing to diverse, and mostly extinct, lineages. All these species have repro- ductive organs that are poorly adapted to wind pollination (the previously presumed mode of reproduction for these taxa). Wind pollination requires that pollen-receptive areas are easily accessible to windborne pollen, which is clearly not the case for these plants. Pollen transfer by insects thus seems most likely, and the scorpionflies are the best candidates so far identified. Some will find these claims controversial, particularly as a key piece of evidence is miss- ing: The authors failed to find any pollen associated with these fossils. This is especially sur- prising for the amber-encased insects, where pollen preserva- tion would be expected ( 11). Absence of evidence is not, however, evidence of absence, and further fossils may provide this information. Biotic pollination was the dominant angiosperm pollina- tion strategy by the late Cre- taceous ( 12). Ren et al.’s research tests old notions that angiosperms evolved in a pre- dominantly wind-pollinated world. Further- more, it challenges us to rethink assumptions that early pollinators were short-tongued gen- eralists that could only exploit open flowers with easily accessible nectar. Living repre- sentatives of the earliest diverging flower- ing plants have a diverse range of pollination systems ( 13), and many are far from general- ized in their interactions with pollinators. The presence of long-tongued pollinating scorpi- onflies both before and at the same time as the first angiosperms allows us to imagine that flowering plants evolved deep flowers early in their radiation, coexisting with open, general- ist flowers and gymnosperms as part of a spe- cialist-generalist spectrum similar to modern plant communities ( 14). Can modern assemblages of plants and pollinators be viewed as analogous to their Mesozoic counterparts, at least in terms of functionality, if not phylogenetic identity? Other Mesozoic insects have been suggested to be fluid-feeding pollinators ( 15, 16), and if this is so, then the scorpionflies described by CREDIT: EMMA COULTHARD/UNIVERSITY OF NORTHAMPTON Landscape and Biodiversity Research Group, School of Applied Sciences, University of Northampton, Park Cam- pus, Northampton NN2 7AL, UK. E-mail: jeff.ollerton@ northampton.ac.uk Ancient legacy. Mesozoic scorpionflies (Mecoptera) probe the female reproductive organs of Leptostrobus cancer, a member of the extinct order Czekanowskiales. Modern scorpionflies are much less diverse than their Mesozoic antecedents. Although they only rarely visit flowers, this habit may be overlooked in modern species and could be a legacy of their distant ancestors. Published by AAAS on November 9, 2009 www.sciencemag.org Downloaded from