Plant Feeding Promotes Diversification in the Crustacea
Total Page：16
File Type：pdf, Size：1020Kb
Plant feeding promotes diversification in the Crustacea Alistair G. B. Poorea,1, Shane T. Ahyongb, James K. Lowryb, and Erik E. Sotkac aEvolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia; bAustralian Museum, Sydney, NSW 2010, Australia; and cGrice Marine Laboratory, College of Charleston, Charleston, SC 29412 Edited by Rodolfo Dirzo, Stanford University, Stanford, CA, and approved July 7, 2017 (received for review April 17, 2017) Abouthalfoftheworld’s animal species are arthropods associated herbivory can explain insect diversification rates varies among with plants, and the ability to consume plant material has been pro- lineages, suggesting that the role of herbivory in promoting di- posed to be an important trait associated with the spectacular diver- versification will be best understood by the examination of a wide sification of terrestrial insects. We review the phylogenetic distribution variety of plant-feeding taxa. of plant feeding in the Crustacea, the other major group of arthropods Here we test whether consuming live plant and macroalgal tissues that commonly consume plants, to estimate how often plant feeding is associated with higher species richness in the Crustacea, the other has arisen and to test whether this dietary transition is associated with major group of arthropods that commonly consumes plant material higher species numbers in extant clades. We present evidence that at (Fig. 1) and the lineage from which insects are derived (18). Crus- least 31 lineages of marine, freshwater, and terrestrial crustaceans taceans are abundant, species rich, and ecologically diverse in most (including 64 families and 185 genera) have independently overcome aquatic systems (21). Herbivorous and omnivorous crustaceans play the challenges of consuming plant material. These plant-feeding clades an important role in ecosystem functioning (22) and can affect the are, on average, 21-fold more speciose than their sister taxa, indicating growth and abundance of primary producers on rocky intertidal that a shift in diet is associated with increased net rates of diversifica- shores (23), in kelp forests (24), seagrass beds (25), salt marshes tion. In contrast to herbivorous insects, most crustaceans have very (26), mangroves (27), freshwater wetlands (28), and in tropical broad diets, and the increased richness of taxa that include plants in forests on land (29). Herbivorous amphipods and isopods are par- their diet likely results from access to a novel resource base rather than ticularly abundant on aquatic macrophytes and have been likened to host-associated divergence. insects because of their feeding mode, use of host plants as both food and shelter, and interactions with producer secondary metab- herbivory | crustaceans | diversification | speciation | arthropods olites (30). In common with herbivorous insects in terrestrial sys- EVOLUTION tems, herbivorous crustaceans in many aquatic systems are a major he origin of novel traits that allow species to use a previously component of secondary production and are an important link to Tunexploited resource is widely used as an explanation for the higher trophic levels (31). Crustacean herbivores did not arise until high species richness in certain lineages of life on Earth. The after the Devonian period, and Vermeij and Lindberg (32) con- hypothesis that these traits can be used to explain the variation in servatively estimated that herbivory arose independently three times species richness among clades in the tree of life has been a major in the isopods, five times in amphipods, and four times in bra- focus of evolutionary biology over the past decades (1, 2). Some chyuran crabs. This repeated and independent evolution of plant of the most influential studies of trait-mediated diversification feeding among the Crustacea gives us an opportunity to test whether have focused on the morphological and behavioral innovations plant feeding is associated with higher species richness in clades that that allow access to a novel food resource and, in particular, the now include plant material in their diets. evolution of herbivory (3). Feeding on plants has long been con- In this study, we first provide a phylogenetic analysis of the sidered an “evolutionary hurdle” (4) because of the low protein distribution of plant feeding across all crustaceans and then use a content of plant material relative to animal tissues and the pres- sister-clade approach to test for shifts in species richness asso- ence of chemical and physical barriers to digesting plant material. ciated with plant feeding. We further test whether an evolutionary shift to plant feeding is associated with an increase in range size or Overcoming those hurdles was central to early hypotheses that geographic distribution. In general, niche breadth is positively plant feeding has promoted the high diversity seen in herbivorous insects (5). Formal tests of this hypothesis provided evidence that the shift to feeding on plant tissue is associated with higher species Significance richness among the highly speciose orders of herbivorous insects (6) and with increased diversification in other organisms, including Understanding what morphological and behavioral traits pro- mammals (7) and dinosaurs (8). mote the success of diverse groups of organisms is a major goal The diversification of insects, in particular, once they began of evolutionary biology. The ability to consume novel food sources feeding on plant material, is thought to have given rise to much of has been linked to the spectacular radiation of herbivorous insects the biological diversity on Earth today (9, 10), and there is an that eat terrestrial plants on Earth. Among the crustaceans, the extensive literature that uses phylogenetic approaches to study the arthropod group that dominates aquatic environments, relatively interaction between insect herbivores and their host plants few major taxa have overcome the challenges of consuming pri- (reviewed in refs. 11, 12). Increased diversity in the butterflies has mary producers (plants and macroalgae). However, lineages that been associated with shifts to feeding on more speciose plant include plant material in their diets support more species than groups (e.g., ref. 13) and to feeding on chemically distinct host their most closely related lineages. The results of our analyses plants (e.g., refs. 14 and 15). Among the beetles, the shift to support the hypothesis that a shift in diet promotes speciation in this diverse and ecologically important animal group. feeding on angiosperms from the species-poor gymnosperms was associated with an increase in species richness by several orders of Author contributions: A.G.B.P., S.T.A., J.K.L., and E.E.S. designed research; A.G.B.P., S.T.A., magnitude, leading Farrell (16) to title his study “Inordinate J.K.L., and E.E.S. performed research; A.G.B.P. and E.E.S. analyzed data; and A.G.B.P., fondness: explained” in reference to J. B. S. Haldane’s well-known S.T.A., and E.E.S. wrote the paper. quote about the astounding diversity of beetles on Earth (17). The authors declare no conflict of interest. More recent analyses, however, have found either that herbivory This article is a PNAS Direct Submission. promotes insect diversification (18) or no evidence for herbivory 1To whom correspondence should be addressed. Email: [email protected]. per se promoting diversification among the beetles (19) and among This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. all insects (3). Wiens et al. (20) showed that the degree to which 1073/pnas.1706399114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1706399114 PNAS | August 15, 2017 | vol. 114 | no. 33 | 8829–8834 Downloaded by guest on September 25, 2021 System (OBIS) database and 2,364 ± 986 records per clade in the GBIF database. The diversity contrast test was robust when the seven contrasts that include the taxa most likely to be data deficient (having fewer than 100 records in the OBIS or GBIF databases, P = 0.023) were removed and when increasing numbers of contrasts were removed at random. The median probability of resampled diversity contrast tests did not exceed 0.05 until 12 randomly selected con- trasts were removed from the total of 26 (Fig. S3). Thus we consider our result robust to the identity of any single contrast or to the possibility that any single sister clade was falsely classified as not plant feeding because of limited knowledge about its diet. Global Distributions of Plant-Feeding Clades. We detected no associ- ation between plant feeding and range sizes, estimated from the number of 1° latitude × 1° longitude blocks in which each species within each clade had been recorded in the GBIF database (ratio t test, t = 0.51, P = 0.61) (Fig. 4B). This result remains unchanged when considering estimates of range size at larger spatial scales (i.e., the number of 5° × 5° and 10° × 10° cells) (all t tests, t < 1.2, Fig. 1. Crustaceans that feed on plants and macroalgae include (A) am- P > 0.2). The larger number of species in the plant-feeding clades phipods (Sunamphitoe femorata living in nests on the giant kelp Macrocystis pyrifera; image: I. Hinojosa), (B) isopods (Amphoroidea typa consuming the resulted in these clades having a larger global distribution, occu- kelp Lessonia spicata), (C) crabs (Hemigrapsus crenulatus grazing on in- pying more 1° × 1° cells in the GBIF database (ratio t test, t = 2.72, tertidal green algae), and (D) crayfish that feed on freshwater macrophytes P = 0.01) (Fig. S4B). (Pacifiastacus leniusculus; image: T. Renals). In both hemispheres the latitudes from which the plant-feeding and their sister clades are found broadly overlap (Fig. 4B). With associated with range size (33), and some explanatory models of insect diversification on higher plants assume that a shift to a broader range of diets will involve an increase in range size (34).