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Diversification and Coevolution in Brood Pollination

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Diversification and Coevolution in Brood Pollination AJB Advance Article published on October 7, 2016, as 10.3732/ajb.1600056. The latest version is at http://www.amjbot.org/cgi/doi/10.3732/ajb.1600056 RESEARCH ARTICLE AMERICAN JOURNAL OF BOTANY INVITED PAPER For the Special Section: The Ecology, Genetics, and Coevolution of Intimate Mutualisms Diversifi cation and coevolution in brood pollination mutualisms: Windows into the role of biotic interactions in generating biological diversity1 David H. Hembry 2,4 and David M. Althoff 3 Brood pollination mutualisms—interactions in which specialized insects are both the pollinators (as adults) and seed predators (as larvae) of their host plants—have been infl uential study systems for coevolutionary biology. These mutualisms include those between fi gs and fi g wasps, yuccas and yucca moths, leaffl owers and leaffl ower moths, globefl owers and globefl ower fl ies, Silene plants and Hadena and Perizoma moths, saxifrages and Greya moths, and senita cacti and senita moths. The high reciprocal diversity and species-specifi city of some of these mutualisms have been cited as evidence that co- evolution between plants and pollinators drives their mutual diversifi cation. However, the mechanisms by which these mutualisms diversify have received less attention. In this paper, we review key hypotheses about how these mutualisms diversify and what role coevolution between plants and pollinators may play in this process. We fi nd that most species-rich brood pollination mutualisms show signifi cant phylogenetic congruence at high taxonomic scales, but there is limited evidence for the processes of both cospeciation and duplication, and there are no unambiguous examples known of strict-sense con- temporaneous cospeciation. Allopatric speciation appears important across multiple systems, particularly in the insects. Host-shifts appear to be common, and widespread host-shifts by pollinators may displace other pollinator lineages. There is relatively little evidence for a “coevolution through cospecia- tion” model or that coevolution promotes speciation in these systems. Although we have made great progress in understanding the mechanisms by which brood pollination mutualisms diversify, many opportunities remain to use these intriguing symbioses to understand the role of biotic interactions in generating biological diversity. KEY WORDS brood pollination; coevolutionary diversifi cation; Ficus ; obligate pollination mutualism; Phyllanthus ; pollinating seed parasite; seed predator; speciation; Yucca Brood pollination mutualisms—specialized interactions in which those between leaffl ower plants and leaffl ower moths ( Kato et al., plants are pollinated by insects which, as larvae, consume seeds of the 2003 ; Kawakita, 2010 ), Silene and two genera of moths, Hadena and same plants—have evolved only a handful of times in the entire co- Perizoma ( Kephart et al., 2006 ), globefl owers and globefl ower fl ies evolutionary history of insects and angiosperms. Despite having ( Pellmyr, 1992 ; Després et al., 2002b ), saxifrages and Greya moths arisen infrequently, these mutualisms can be extraordinarily species- ( Pellmyr and Th ompson, 1992 ), and senita cacti and senita moths rich and ecologically dominant in some ecosystems and have long ( Fleming and Holland, 1998 ). Th ese interactions have been enor- attracted attention from natural historians, evolutionary biologists, mously important study systems for the evolution of cooperation and and ecologists. Th e most famous of these mutualisms are those be- for coevolutionary biology. In this review, we consider the evidence tween fi gs and fi g wasps ( Mayr, 1885 ; Cook and Rasplus, 2003 ) and for the mechanisms of diversifi cation of both plants and insects en- yuccas and yucca moths ( Riley, 1892 ; Pellmyr, 2003 ); others include gaged in brood pollination mutualisms, and the role of biotic interac- tions (and coevolution) in that diversifi cation. 1 Manuscript received 6 February 2016; revision accepted 10 May 2016. In the same way that one might study anoles, cichlids, or Galápa- 2 Department of Ecology and Evolutionary Biology, University of Arizona, P. O. Box 210088, gos fi nches to understand adaptive radiation, brood pollination Tucson, Arizona 85721 USA; and mutualisms (also sometimes referred to as nursery pollination mu- 3 Department of Biology, Syracuse University, 107 College Place, Syracuse, New York, 13244 tualisms, pollinating seed-predation mutualisms, pollinating seed- USA 4 Author for correspondence (e-mail: [email protected]), phone: +1-520-626- parasite mutualisms, and in the case of fi gs, yuccas, and leaffl owers, 9315 obligate pollination mutualisms) have been major study systems for doi:10.3732/ajb.1600056 understanding coevolutionary diversifi cation. We choose the term AMERICAN JOURNAL OF BOTANY 103 (10): 1 – 10 , 2016; http://www.amjbot.org/ © 2016 Botanical Society of America • 1 Copyright 2016 by the Botanical Society of America 2 • AMERICAN JOURNAL OF BOTANY brood pollination over other, widely used synonyms in this synthesis In this review, we ask how brood pollination interactions diver- because of its brevity (relative to pollinating seed-predation mutu- sify, and then use this evidence to ask what the role of biotic inter- alism), because fi g wasp larvae technically are infl orescence gallers actions between plants and pollinators (including coevolution) is in rather than seed predators, and also because we wish to compare pro- this diversifi cation process. Th roughout, we will suggest key hy- cesses in otherwise analogous interactions that diff er in whether they potheses that need to be tested to strengthen the link between co- are strictly obligate or include copollinators (below). evolution and diversifi cation. Approaches that focus on coevolution Here we defi ne coevolutionary diversifi cation broadly as diversi- per se have been criticized both for their unworkability (coevolu- fi cation (among populations, species, or clades) in which coevolu- tion is diffi cult to demonstrate) and on empirical and theoretical tion (reciprocal natural selection sensu Janzen, 1980 ; Th ompson, grounds (there is little, or mixed, evidence for coevolution promot- 2005 ) drives the diversifi cation (sensu Hembry et al., 2014 ; ing diversifi cation, particularly in mutualisms) ( Yoder and Nuismer, note that this is a broader defi nition than that of Althoff et al., 2010 ; Hembry et al., 2014 ). We note therefore that our approach 2014 ). Importantly, coevolutionary diversifi cation may not neces- off ers a more nuanced perspective that is informative whether the sarily create phylogenetic congruence between coevolving clades goal is to emphasize the role of biotic interactions more generally or ( Th ompson, 2005 ; Poisot, 2015 ). Th is emphasis on brood pollina- coevolution specifi cally in diversifi cation. Specifi cally, we ask the tion mutualisms is due to four characteristics many of these sys- following questions: how specialized (at the species level) are plants tems share: (1) the highly intertwined life cycles of both plants and and brood pollinators to each other, do they diversify through co- pollinators, (2) the fact that the pollinators control most (if not all) speciation or some other process that generates phylogenetic con- pollen fl ow in their plant hosts ( Th ompson, 1994 ), (3) the great de- gruence, do they speciate in allopatry, do pollinator clades displace gree of species-level specialization seen between plants and pollina- each other competitively, and is coevolution implicated in either tors in nature ( Wiebes, 1979 ; Weiblen, 2002 ; Kawakita and Kato, plant or insect speciation? 2006 ; Althoff et al., 2012 ), and (4) the high species richness in some plant and pollinator clades engaged in these interactions ( Janzen, 1979 ; Kawakita, 2010 ). Although the hypothesis that coevolution WHAT ARE THE BROOD POLLINATION MUTUALISMS? promotes diversifi cation has been invoked for a wide number of organisms and types of interactions ( Ehrlich and Raven, 1964 ; Dietl We defi ne brood pollination mutualisms as mutualisms in which and Kelley, 2002 ; Th ompson, 2005 , 2009 ; Hembry et al., 2014 ), the larvae of pollinators consume seeds or other female infl orescence above attributes of brood pollination mutualisms make them ideal tissue. Brood pollination mutualisms involve diverse taxa from test cases for this hypothesis. many diff erent geographic areas ( Table 1 ). Th ese interactions are Despite the fact that they have been major and infl uential study usually obligate, but in some systems they can be more facultative systems for understanding the role of coevolution (or biotic inter- at least for the plants. For instance, fi gs, yuccas, and leaffl owers are actions more generally) in diversifi cation, we know very little about generally described in the literature as obligately pollinated by their the mechanisms by which the plants and insects engaged in brood respective brood pollinators (obligate pollination mutualisms; e.g., pollination mutualisms diversify. Th is defi ciency is largely due to Pellmyr, 2003 ; Kawakita, 2010 ). In contrast, it is well established the patterns of diversity across the diff erent brood pollination mu- that the senita cactus is not exclusively pollinated by senita moths tualisms. Some of these interactions (e.g., fi gs, leaffl owers) have ( Holland and Fleming, 1999 ) and Silene – Hadena, Silene – Perizoma , hundreds of species, primarily in the tropics ( Berg, 1989 ; Kawakita, and Lithophragma – Greya interactions both
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