Abstract
Geographic isolation is the first step in insect herbivore diet specialization. Such specialization is postulated to increase insect fitness, but may simultaneously reduce insect ability to colonize novel hosts. During the Paleocene-Eocene, plants from the order Zingiberales became isolated either in the Paleotropics or in the Neotropics. During the Cretaceous, rolled-leaf beetles diversified in the Neotropics concurrently with Neotropical Zingiberales. Using a community of Costa Rican rolled-leaf beetles and their Zingiberales host plants as study system, we explored if previous geographic isolation precludes insects to expand their diets to exotic hosts. We recorded interactions between rolled-leaf beetles and native Zingiberales by combining DNA barcodes and field records for 7450 beetles feeding on 3202 host plants. To determine phylogenetic patterns of diet expansions, we set 20 field plots including five exotic Zingiberales, recording beetles feeding on these exotic hosts. In the laboratory, using both native and exotic host plants, we reared a subset of insect species that had expanded their diets to the exotic plants. The original plant-herbivore community comprised 24 beetle species feeding on 35 native hosts, representing 103 plant-herbivore interactions. After exotic host plant introduction, 20% of the beetle species expanded their diets to exotic Zingiberales. Insects only established on exotic hosts that belong to the same plant family as their native hosts. Laboratory experiments show that beetles are able to complete development on these novel hosts. In conclusion, rolled-leaf beetles are pre-adapted to expand their diets to novel host plants even after millions of years of geographic isolation.
Keywords: Cephaloleia, Costa Rica, diet expansions, DNA barcoding, ecological fitting, herbivory, La Selva Biological Station, phylogenetic constraints
In phytophagous insects, diet expansions to novel hosts are usually phylogenetically conservative (Goβner et al. 2009). This tendency of insects to expand their diets to closely related hosts is a byproduct of resource tracking, co-speciation, and in some cases, coevolution (Ehrlich & Raven 1964, Janzen 1980, Futuyma & Moreno 1988). After insects evolved metabolic adaptations to the unique set of chemical defenses of a particular group of host plants, phylogenetic inertia is expected to reduce insect ability to expand their diets to host plants from distant clades, which usually display different secondary compounds (Nosil 2002).
During the Paleocene-Eocene (~65 – 35 MY), many tropical plant clades became isolated in landmasses that today we know as the Paleotropics and the Neotropics (Raven & Axelrod 1974). In geographic isolation, host plants together with their insect herbivores started independent adaptive radiations (Pellmyr et al. 1998, Percy et al. 2004, Heikkilä et al. 2012).
At present, human-driven introductions of exotic plants and insects are generating the breakdown of geographic barriers between Paleotropical and Neotropical lineages (Verhoeven et al. 2009). These encounters between previously isolated biotas represent a unique opportunity to explore the role of phylogenetic conservatism, adaptation and preadaptation on the assemblage of novel plant-herbivore interactions (Strauss et al. 2006).
One group of plants of Cretaceous origin is the order Zingiberales (124 ± 3 MY) (Kress 1990, Kress et al. 2001). This order includes plants of economic importance such as banana (family Musaceae), ginger (family Zingiberaceae), and many ornamental plants in the families Cannaceae, Costaceae, Heliconiaceae, Marantaceae, Lowiaceae, and Strelitziaceae (Kress 1990). Most Zingiberales families originated between 110 – 95 MY ago (Kress et al. 2001, Kress & Specht 2006).
After the Gondwana vicariance and several long-distance colonization events, members of the families Costaceae, Marantaceae, Strelitziaceae, and Zingiberaceae evolved while isolated both in the Paleotropics and Neotropics (Kress et al. 2001). The family Musaceae radiated in isolation in the Paleotropics. In the Neotropics, the families Cannaceae and Heliconiaceae diversified ca. 30 MY ago (Kress & Specht 2006).
In the Neotropics, a group of insect herbivores, Cephaloleia and Chelobasis beetles (Coleoptera: Chrysomelidae) started an adaptive radiation with their hosts, Neotropical plants in the Zingiberales (Wilf et al. 2000). Cephaloleia and Chelobasis beetles are also known as the rolled-leaf beetles because their life cycle is completed inside the scroll formed by the young rolled leaves of their host plants (Staines & Garcia-Robledo 2014). At present, 97 of the 214 known species of Cephaloleia species have been recorded feeding on Neotropical Cannaceae, Costaceae, Heliconiaceae, Marantaceae, and Zingiberaceae (Staines & Garcia-Robledo 2014). Feeding records for Chelobasis only include plants in the family Heliconiaceae (Staines & Garcia-Robledo 2014).
The central objective of the study described in this paper was to determine whether Neotropical rolled-leaf beetles can successfully utilize exotic Zingiberales as hosts. We selected a speciose community of rolled-leaf beetles at La Selva Biological Station (Costa Rica, Central America) as a study system. We first determined the taxonomy and original (native) diets of all the insect species in this group at this site. To delimit insect species, we combined traditional taxonomy with DNA barcoding methods, and recorded the associations between rolled-leaf beetles and host plants during two years.
To determine if rolled-leaf beetles are able to recognize and complete their life cycle on novel host plants, we introduced four Asian and one South American exotic species of Zingiberales to La Selva and observed the occurrence of rolled-leaf beetles on these potential host plants. These exotic species were already present on the Atlantic slope of Costa Rica, but are rare inside La Selva. One possible outcome was that insect adaptation to Neotropical Zingiberales during the last 40–60 MY would prevent them from recognizing Asian Zingiberales as potential hosts (Wilf et al. 2000, Garcia-Robledo & Staines 2008). Alternatively, some of the rolled-leaf beetle species might recognize Asian Zingiberales as potential hosts. If rolled-leaf beetles (which are only Neotropical) could complete their life cycles on Asian Zingiberales, this is would constitute an example of the enormous potential for colonization and assembly of novel interactions in insect herbivores. In this context, we addressed the following questions: (1) Are diet expansions to novel hosts restricted due to phylogenetic conservatism and the lack of an adaptive radiation with plant clades from non-native biogeographical regions? and (2) Are insect herbivores preadapted, thus able to complete their life cycle on novel hosts after 110 million years of host plant divergence?
METHODS
Study site and species
This study was conducted at La Selva Biological Station (hereafter La Selva), a tropical rain forest in Central America between 2008 and 2015 (McDade 1994). The study site is located in the lowlands of Costa Rica and has an elevational range of 35 to 137 m. a.s.l. and rainfall variability of 152.0 mm in March to 480.7 mm in July. At La Selva there are 20 morphologically distinct rolled-leaf beetle species and 33 species of native Zingiberales belonging to the families Heliconaceae, Costaceae, Zingiberaceae, Cannaceae, and Marantaceae (García-Robledo et al. 2013).
For field and laboratory experiments testing the potential of rolled-leaf beetles to use exotic plants as hosts, we selected five plant species. Musa velutina (Musaceae), native to India, Heliconia psittacorum (Heliconiaceae), native to the Caribbean and northern South America, Alpinia purpurata and Hedychium coronarium (Zingiberaceae), natives to the Pacific Islands and India, and Cheilocostus speciosus (Costaceae), native to India (García-Robledo & Horvitz 2012). All these exotic Zingiberales had previously been introduced in the Caribbean lowlands around three decades ago as ornamentals (García-Robledo & Horvitz 2012). At La Selva, a few individuals of Ch. speciosus, H. psittacorum and A. purpurata and naturalized populations of H. coronarium and M. velutina had previously been recorded in secondary forest and removed by the La Selva exotic plant management program (García-Robledo & Horvitz 2012).
Identification of rolled-leaf beetle species using traditional taxonomy and DNA barcoding
To identify rolled-leaf beetle species present at La Selva, we collected 896 individuals. Beetles were independently identified by two taxonomists (C.L.S. and C.G.R) using morphological characters. In addition, to identify potential cryptic species, we amplified the DNA barcode Cytochrome C Oxidase Subunit 1 (CO1) for a subset of 397 individuals that included representatives of all morphological species collected on each host plant at La Selva.
Beetles used for molecular analyses were collected in ET-OH 95%. DNA extraction and amplification of CO1 sequences were performed following protocols by Garcia-Robledo et al. (García-Robledo et al. 2013). DNA sequences were aligned using MUSCLE (Edgar 2004). We generated a neighbor-joining phylogenetic tree and estimated bootstrap support after 100 replicates using GENEIOUS PRO, v. 5.6.5 (Biomatters-development-team 2012). Chelobasis bicolor (Gray, 1832) and Chelobasis perplexa (Baly, 1858) (Chrysomelidae) were selected as the outgroup.
Determining original insect diets using field records
To determine the diet breadths of rolled-leaf beetles at La Selva, we surveyed 3202 young rolled leaf scrolls and recorded all the rolled-leaf beetles found in each for a total of 7450 beetles. We performed these surveys during the transition from the dry to rainy season (January–March) of the years 2008 and 2010.
Based on these records, we determined the contribution of each host plant to the overall diet breadth of each beetle species. We estimated the relative importance of each host plant in the overall diet breadth of each beetle species by calculating the average density of individuals of each herbivore species per rolled leaf for each host plant species Īij:
| (Equation 1) |
Where Iij is the total number of individual insects of species i found on all individuals of host plant j and Pj is the total number of rolled leaves surveyed for each host plant species j. To determine diet similarities among rolled-leaf beetles, we generated a matrix containing values of Īij for each interaction, and then performing a Bray-Curtis dissimilarity hierarchical cluster analysis (R-Development-Core-Team 2009).
Experimental diet expansions to novel host plants
To determine if rolled-leaf beetles would find and feed upon exotic Zingiberales, we established 20 experimental plots in the field. The minimum distance among plots was 200 m. In each plot we planted one individual of each of five exotic plant species: Musa velutina (Musaceae), Heliconia psittacorum (Heliconiaceae), Alpinia purpurata and Hedychium coronarium (Zingiberaceae), and Cheilocostus speciosus (Costaceae). Plants were placed in individual 5-gallon pots, each pot placed at a minimum distance of 2 m from any other. Each plant was visited every week and reproductive structures were removed to prevent escape of genes or propagules into the wild. We recorded the presence of rolled-leaf beetles feeding in the new leaf scrolls of the plants. Beetles were collected in ET-OH 95% for further identification. Plants were surveyed for three months, after which, all exotic plants in the experimental plots were removed from the field.
We performed two statistical analyses to determine if rolled-leaf beetles that feed on hosts from multiple plant families, or insects with more host plant species included in their diets are more likely to expand their diets to exotic hosts. To determine if there is an association between the number of host plant families consumed by each insect species and the probability of diet expansions to exotic hosts, we performed a contingency analysis (Zar 1999). To explore a relationship between the number of host plant species and diet expansions to novel hosts, we performed a logistic regression between the number of host species consumed and the presence/absence of each insect species on exotic hosts (Zar 1999).
Phylogenetic constraints in rolled-leaf beetle diet expansions to novel hosts
To determine if diet expansion onto novel hosts is phylogenetically constrained, we generated a chronogram of the tempo and mode of evolution of the main clades of Zingiberales. Time of divergence between clades is based on fossil records, molecular data and geological information (Kress 1984, 1990, Kress et al. 2001, Kress & Specht 2006, Prince & Kress 2006). Using the chronogram including both Paleotropical and Neotropical clades, we estimated the time since divergence of the native and exotic plant species.
Development time and survival of rolled-leaf beetles on native and novel host plants
To determine if rolled-leaf beetle species can complete their life cycle on novel host plants, we selected Cephaloleia belti, C. dorsalis (hap 1), C. placida, Cephaloleia sp. nov., (see Figure 3). We collected gravid females in the field (NC. belti = 38, NC. dorsalis hap1 = 37, N C. placida = 42, N Cephaloleia sp. nov. = 32). Females were fed ad libitum with leaf tissue from their most frequently used host plant (Figs. 2 and 3). Eggs were placed in individual containers, and after eclosion, larvae were fed with leaf tissue from either native or the novel host plants.
FIGURE 3.
Diet expansions of rolled-leaf beetles and time of divergence between their native and novel host plants. Chronogram shows time of origin of rolled-leaf and main diversification events of their Zingiberales host plants: A. Origin of Musaceae. B. Diversification of Zingiberaceae. C. Origin of Cephaloleia rolled-leaf beetles and radiation of Neotropical and Paleotropical Costaceae. D. Diversification of Heliconiaceae. Bipartite network represents interactions among rolled-leaf beetles and their main native and novel host plants. Species abbreviations: RA: Renealmia alpinia, AP: Alpinia, HC: Hedychium coronarium (Zingiberaceae). CM: Costus malortieanus, CS: Cheilocostus speciosus (Costaceae), HL: Heliconia latispatha, HP: Heliconia psittacorum (Heliconiaceae), Musa velutina, (Musaceae). SP: Cephaloleia sp. Nov. TR: C. trimaculata, PL: C. placida, DO: C. dorsalis hap 1. BE: C. belti, CO: C. congener, RE: C. reventazonica.
FIGURE 2.
Diet similarities among rolled-leaf beetles at La Selva Biological Station. The matrix represents the relative contribution of each host plant to the overall diet breadth of each species of herbivorous insect (Equation 1). Numbers on the nodes are used to describe in the text patterns of host plant use of herbivorous insects. Species of herbivorous insects are grouped using a Bray-Curtis dissimilarity hierarchical cluster analysis.
For each species, we estimated the time to pupation when reared on each host plant species. We also recorded the number of individuals that completed their life cycle and emerged as adults on each host plant species. Differences in development time among insects reared on native or novel hosts were tested using non-parametric Kruskal Wallis and Wilcoxon tests. Differences in the proportion of adults emerging from each host plant species were determined using chi-square and a-posteriori tests (Package fifer in the statistical program/software R). All analyses were performed using program R (R-Development-Core-Team 2009).
RESULTS
Identification of rolled-leaf beetle species using traditional taxonomy and DNA barcoding
We found 20 morphologically distinct rolled-leaf beetle species and four cryptic species complexes revealed by DNA barcoding (Fig. 1). The cryptic species included species with specialized diets that feed on a single host plant (e.g., Ch. perplexa haplotype 1, Cephaloleia sp. nov), generalists that feed on several plant families (e.g., C. dilaticollis), and even species that feed on other plant orders (e.g., the C. trivittata complex) (Fig. 2).
FIGURE 1.
Identification of rolled-leaf beetle species at La Selva Biological Station using the DNA barcode CO1. Haplotypes (hap.) represent cryptic species based on sequence differences in the DNA barcode CO1. (GenBank submission: dx.doi.org/10.5883/DS-BOFCR, accession nos. KU357054–KU358485).
Chelobasis perplexa and Cephaloleia trivittata represent two haplotypes (Figure 1). We also recorded a cryptic species complex for Cephaloleia dorsalis that is represented by three different haplotypes (Fig. 1). We found no evidence of cryptic species complexes for other rolled-leaf beetle species, including the most generalist species, Cephaloleia belti and C. reventazonica (Fig. 1).
Determining original insect diets of rolled-leaf beetles
Most of the beetle species were specialists, feeding on a single plant family (19 beetle species) or even a single plant species (seven beetle species) (Fig. 2). Even the most generalist species fed predominantly on one or a few host plants (Fig. 2).
Most beetles specialized on Heliconiaceae (Fig. 2, node 1), Marantaceae (Figure 2, Node 2), Costaceae (Fig. 2, node 3) or Zingiberaceae (Fig. 2, node 4). Five beetle species fed on multiple host plant families. We also recorded two beetle species feeding on non-Zingiberaceous species in the families Poaceae and Cyclanthaceae (Fig. 2).
Phylogenetic constraints in rolled-leaf beetle diet expansions to novel hosts
In the experimental plots, we observed that seven rolled-leaf beetle species had expanded their diets to include exotic hosts (Table S1). Diet expansions of all rolled-leaf beetle species were phylogenetically conservative (Fig. 3). We did not generally find that insect species expanded their diets beyond the family of their native host plants (Fig. 3). The exceptions were three species of Cephaloleia (C. belti, C. congener and C. reventazonica) that expanded their diets from Heliconiaceae to Musa in the Musaceae, a neighboring family.
There is no association between the number of host plant families consumed by rolled-leaf beetles and the probability of diet expansion to novel hosts (X2 df =2, N = 24 = 2.07, P = 0.35). Also, there is no association between number of host plant species and diet expansions to novel hosts (R2 = 0.07357, df = 1,20, P = 0.51).
Development time and survival of rolled-leaf beetles on native and novel host plants
Larvae reared on native hosts displayed shorter time to pupation than larvae reared on novel hosts (Fig. 4). Time to pupation for Cephaloleia belti, Cephaloleia sp. nov and C. dorsalis on novel hosts was one to two weeks longer than on native hosts. Time to pupation in C. placida was more than three times longer for larvae reared on novel hosts than on their native hosts (Fig. 4).
FIGURE 4.
Development time from eclosion to pupation of four rolled-leaf beetle species reared on native and novel hosts (Median ± 3rd quartile, 95% CI). A. Cephaloleia belti B. Cephaloleia sp. nov. C. Cephaloleia dorsalis hapltype 1 D. Cephaloleia placida.
The proportion of individuals that completed their development to adults was higher for larvae reared on native than on novel hosts (Fig. 5). Although development on some host plants was particularly challenging, and mortality was higher than 90% (e.g., Cephaloleia sp. nov and C. placida larvae reared on Hedychium coronarium) (Fig. 5), we recorded some individuals of each rolled-leaf beetle species that completed their development when feeding on novel hosts (Fig. 5).
FIGURE 5.
Proportion of Cephaloleia larvae that completed their development to adults when feeding on native or novel host plants. Numbers on the bars = sample size. Letters above bars represent similarity among groups. A. Cephaloleia belti B. Cephaloleia sp. nov. C. Cephaloleia dorsalis hapltype 1 D. Cephaloleia placida.
DISCUSSION
A central challenge to studying plant-herbivore interaction is the limited taxonomic information available to identify interacting species (Cardoso et al. 2011). Previous studies using DNA barcoding demonstrated that this taxonomic impediment is a serious issue in the tropics, as many morphological species might include cryptic species complexes (Hebert et al. 2004, Kress et al. 2015). Using the DNA barcode CO1 we recorded four cryptic species complexes at La Selva that included nine beetle species with contrasting diet breadths. This study demonstrates that if species identifications were not complemented with molecular tools, our results showing strong phylogenetic conservatism in diet expansions would have been obscured in a limited knowledge of rolled-leaf beetle species boundaries. For example, Cephaloleia sp. nov, C. dorsalis, C. belti, C. congener and C. reventazonica, species recorded expanding their diets to novel hosts are included in cryptic species complexes previously assumed to display broader diets and elevational distributions (García-Robledo et al. 2016).
In this study, we evaluated the potential for shifts to novel hosts in a group of tropical insect herbivores with well-known phylogenetic and biogeographic history (Kress 1990, Wilf et al. 2000, Kress et al. 2001, McKenna & Farrell 2005). One hypothesis we explored was that in adapting to Neotropical Zingiberales, rolled-leaf beetles (all of which are exclusively Neotropical) may have become specialized to the extent that they would not recognize Paleotropical Zingiberales. Our data from a field experiment did not support this hypothesis; they showed that seven native Cephaloleia species were attracted to rolled leaves of one Neotropical and five Paleotropical exotic Zingiberales within 3 months of their being introduced into the wild.
Host shifts are broadly documented in plant crops, such as rice and cacao, and in invasive plants (Strong 1974, 1979). Novel plant-herbivore interactions are usually phylogenetically conservative because closely related plants display similar leaf chemistry used as cues by insect herbivores (Becerra 1997, Bernays 1998). However, insects may also expand their diets to hosts from distant plant clades, but with similar chemical composition (Agrawal 2007).
Plants from different Zingiberales families share leaf chemistry, including those used by rolled-leaf beetles as cues to track their host plants (Merh 1982, Garcia-Robledo & Horvitz 2009). The phylogenetic conservatism of host shifts in rolled-leaf beetles suggests that this group of insect herbivores (which is only found in the Neotropics) is using chemical cues within plant families that are ancestral and pre-date the divergence of plants into Neotropical vs Paleotropical clades. The vicariance event that isolated Neotropical from Paleotropical Zingiberales pre-dates the origin of rolled-leaf beetles (Specht et al. 2002). Therefore the chemistry evolved prior to rolled-leaf beetle radiation in the Neotropics and did not co-evolve with the beetles.
Our data reveal that rolled-leaf beetles are pre-adapted to detect, colonize and complete their life cycles on exotic hosts that are in the same family as their native hosts (Garcia-Robledo & Horvitz 2011, García-Robledo & Horvitz 2012). This suggests that the scenario of coevolution or codiversification proposed by previous studies is unlikely (McKenna & Farrell 2005, Suchan & Alvarez 2015).
The time of diversification of rolled-leaf beetles based on molecular data suggests that rolled-leaf could diversify at least 20 MY after the main radiations of Neotropical Zingiberales (Gómez-Zurita et al. 2007). Thus the novel interactions we observed were assembled through a process known as ‘ecological fitting’, in which organisms colonize novel environments using the suit of traits that they carried at the time they encountered a novel environment rather than by evolving new trait variants (Agosta 2006, Agosta & Klemens 2008).
Our results have broad implications regarding the interpretation of one of the central hypothesis addressing the mechanisms involved in plant-herbivore diversification—i.e., the coevolution—escape and radiate hypothesis (Ehrlich & Raven 1964, Janzen 1980, Futuyma & Moreno 1988). If speciation events of Zingiberales and associated herbivores were driven by the arms race proposed by this hypothesis, one prediction would be that rolled-leaf beetle expansions to Paleotropical hosts should be unlikely. Our results illustrate how the combination of conservative plant chemistry together with the immense plasticity of insect herbivore diets facilitate diet expansions to nove hosts. This study also highlights the relevance of alternative processes such as preadaptation and resource tracking in the evolution and assembly of plant insect interactions.
Novel host plants represent challenging environments for rolled-leaf beetles in the sense that larval development time is longer and mortality is higher than on native host plants (Garcia-Robledo et al. 2010). This study shows that although novel interactions between rolled-leaf beetles and Zingiberales are assembled through ecological fitting, insect herbivores would likely have to adapt and evolve over generations to attain fitness on novel hosts which is equivalent to their fitness on native hosts.
Humans are modifying species composition of natural areas by introducing non-native species (Maron & Vila 2001). As a result, the assembly of novel plant-herbivore interactions is a global phenomenon (Saul & Jeschke 2015). Recent studies show that because insect herbivore diet expansions are phylogenetically conservative, it is possible to predict novel associations based on native insect diets and evolutionary relationships among native and novel hosts (Pearse & Altermatt 2013).
In conclusion, adaptation of rolled-leaf beetles to Neotropical families of Zingiberales promote phylogenetic conservatism and constrains diet expansions to plants in the same families. However, this specialization does not represent an evolutionary dead end. Rolled leaf beetles are pre-adapted to be able to expand their diets to novel hosts that are in the same family as native hosts, even after millions of years of geographic isolation.
Supplementary Material
Acknowledgments
The authors thank the staff of La Selva Biological Station - Organization for Tropical Studies. We want to thank G. Frias, J.G. Huertas, G. Huertas and R. Sanchez, for assistance in the field and laboratory. We are grateful to E.K. Kuprewicz and two anonymous reviewers of this manuscript for their constructive suggestions. We also want to thank the J. McLamore Fellowship - University of Miami and the OTS (Organization for Tropical Studies)—Donald and Beverly Stone and Christiane and Christopher Tyson Fellowships, the Smithsonian Institution Postdoctoral Fellowship Program, Global Earth Observatories Program, and the Office of the Under Secretary for Science, and the National Geographic/Waitt Institute Grant (W149-11) to C.G-R the Smithsonian Pell Grant to T.L.E (with collaborators W.J.K. and C.G-R), the Cooper Fellowship, College of Arts and Sciences, University of Miami, the US National Institutes of Health, National Institute of Aging P01 AG022500-01 and NSF DEB-0614457 grants to C.C.H.
Footnotes
DATA AVAILABILITY
Data available in the Dryad Repository: http://dx.doi.org/10.5061/dryad.7nk99 (Garcia-Robledo et al. 2017). The DNA sequences reported in this paper have been deposited in the GenBank database, dx.doi.org/10.5883/DS-BOFCR (accession nos. KU357054 – KU358485). Development times and percent of emergence estimates are part of the quatitative genetics datasets of: García-Robledo C, Horvitz CC (2011). Journal of Evolutionary Biology 25(1): 38–53. Dataset available in dryad: http://dx.doi.org/10.5061/dryad.c0s0h763. Dataset 1. Matrix of quantitative interactions used to generate cluster analysis (Fig. 2); Dataset 2. Data to generate Figure 4 (Time to pupation of rolled-leaf beetles reared on native and novel hosts); Dataset 3. Data to generate Figure 5 (Proportion of emergence of adult rolled-leaf beetles reared on native and novel hosts).
Additional Supporting Information may be found online in the supporting information tab for this article:
TABLE S1. Rolled-leaf beetle species attracted to novel Zingiberales host plants at La Selva Biological Station, Costa Rica.
LITERATURE CITED
- Agosta SJ. On ecological fitting, plant-insect associations, herbivore host shifts, and host plant selection. Oikos. 2006;114:556–565. [Google Scholar]
- Agosta SJ, Klemens JA. Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution. Ecol Lett. 2008;11:1123–1134. doi: 10.1111/j.1461-0248.2008.01237.x. [DOI] [PubMed] [Google Scholar]
- Agrawal AA. Macroevolution of plant defense strategies. TREE. 2007;22:103–109. doi: 10.1016/j.tree.2006.10.012. [DOI] [PubMed] [Google Scholar]
- Becerra JX. Insects on plants: macroevolutionary chemical trends in host use. Science. 1997;276:253–256. doi: 10.1126/science.276.5310.253. [DOI] [PubMed] [Google Scholar]
- Bernays EA. Evolution of feeding behavior in insect herbivores. Bioscience. 1998;48:35–44. [Google Scholar]
- Biomatters-development-team. Geneious® Pro 5.6.5. created by Biomatters. 2012 Available from http://www.biomatters.com/
- Cardoso P, Erwin TL, Borges PA, New TR. The seven impediments in invertebrate conservation and how to overcome them. Biol Conserv. 2011;144:2647–2655. [Google Scholar]
- Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ehrlich PR, Raven PH. Butterflies and plants: a study in coevolution. Evolution. 1964;18:586–608. [Google Scholar]
- Futuyma DJ, Moreno G. The evolution of ecological specialization. Annu Rev Ecol Evol Syst. 1988;19:207–233. [Google Scholar]
- García-Robledo C, Erickson DL, Staines CL, Erwin TL, Kress WJ. Tropical plant–herbivore networks: reconstructing species interactions using DNA barcodes. PLoS One. 2013;8:e52967. doi: 10.1371/journal.pone.0052967. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Garcia-Robledo C, Horvitz CC. Host plant scents attract rolled-leaf beetles to Neotropical gingers in a Central American tropical rain forest. Entomol Exp Appl. 2009;131:115–120. [Google Scholar]
- Garcia-Robledo C, Horvitz CC. Experimental demography and the vital rates of generalist and specialist insect herbivores on native and novel host plants. J Anim Ecol. 2011;80:976–989. doi: 10.1111/j.1365-2656.2011.01843.x. [DOI] [PubMed] [Google Scholar]
- García-Robledo C, Horvitz CC. Parent–offspring conflicts,”optimal bad motherhood” and the “mother knows best” principles in insect herbivores colonizing novel host plants. Ecol Evol. 2012;2:1446–1457. doi: 10.1002/ece3.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Garcia-Robledo C, Horvitz CC, Kress WJ, Carvajal-Acosta AN, Erwin TL, Staines CL. Dryad Digital Repository. 2017. Data from: Experimental assemblage of novel plant-herbivore interactions: ecological host shifts after 40 million years of isolation. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Garcia-Robledo C, Horvitz CC, Staines CL. Larval morphology, development, and notes on the natural history of Cephaloleia “rolled-leaf” beetles (Coleoptera: Chrysomelidae: Cassidinae) Zootaxa. 2010;2610:50–68. [Google Scholar]
- García-Robledo C, Kuprewicz EK, Staines CL, Erwin TL, Kress WJ. Limited tolerance by insects to high temperatures across tropical elevational gradients and the implications of global warming for extinction. Proceedings of the National Academy of Sciences. 2016;113:680–685. doi: 10.1073/pnas.1507681113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Garcia-Robledo C, Staines CL. Herbivory in gingers from latest Cretaceous to present: is the ichnogenus Cephaloleichnites (Hispinae, Coleoptera) a rolled-leaf beetle? J Paleontol. 2008;82:1035–1037. [Google Scholar]
- Gómez-Zurita J, Hunt T, Kopliku F, Vogler AP. Recalibrated tree of leaf beetles (Chrysomelidae) indicates independent diversification of angiosperms and their insect herbivores. PLoS ONE. 2007:2. doi: 10.1371/journal.pone.0000360. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goβner MM, Chao A, Bailey RI, Prinzing A. Native fauna on exotic trees: phylogenetic conservatism and geographic contingency in two lineages of phytophages on two lineages of trees. Am Nat. 2009;173:599–614. doi: 10.1086/597603. [DOI] [PubMed] [Google Scholar]
- Hebert PD, Penton EH, Burns JM, Janzen DH, Hallwachs W. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA. 2004;101:14812–14817. doi: 10.1073/pnas.0406166101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heikkilä M, Kaila L, Mutanen M, Peña C, Wahlberg N. Cretaceous origin and repeated tertiary diversification of the redefined butterflies. P Roy Soc B-Biol Sci. 2012;279:1093–1099. doi: 10.1098/rspb.2011.1430. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Janzen DH. When is it coevolution. Evolution. 1980;34:611–612. doi: 10.1111/j.1558-5646.1980.tb04849.x. [DOI] [PubMed] [Google Scholar]
- Kress WJ. Systematics of Central American Heliconia (Heliconiaceae) with pendent inflorescences. J Arnold Arboretum. 1984;65:429–532. [Google Scholar]
- Kress WJ. The phylogeny and classification of the Zingiberales. Ann Mo Bot Gard. 1990;77:698–721. [Google Scholar]
- Kress WJ, García-Robledo C, Uriarte M, Erickson DL. DNA barcodes for ecology, evolution, and conservation. TREE. 2015;30:25–35. doi: 10.1016/j.tree.2014.10.008. [DOI] [PubMed] [Google Scholar]
- Kress WJ, Prince LM, Hahn WJ, Zimmer EA. Unraveling the evolutionary radiation of the families of the Zingiberales using morphological and molecular evidence. Syst Biol. 2001;50:926–944. doi: 10.1080/106351501753462885. [DOI] [PubMed] [Google Scholar]
- Kress WJ, Specht CD. The evolutionary and biogeographic origin and diversification of the tropical monocot order Zingiberales. Aliso. 2006;22:619–630. [Google Scholar]
- Maron JL, Vila M. When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos. 2001;95:361–373. [Google Scholar]
- McDade LA. La Selva: ecology and natural history of a neotropical rain forest. University of Chicago Press; 1994. [Google Scholar]
- McKenna DD, Farrell BD. Molecular phylogenetics and evolution of host plant use in the Neotropical rolled leaf ‘hispine’ beetle genus Cephaloleia (Chevrolat) (Chrysomelidae : Cassidinae) Mol Phylogenet Evol. 2005;37:117–131. doi: 10.1016/j.ympev.2005.06.011. [DOI] [PubMed] [Google Scholar]
- Merh PS. PhD Dissertation. Maharaja Sayajirao University of Baroda; Vadodara, India: 1982. Taxonomy and chemistry of some members of Zingiberales and Cyperales. [Google Scholar]
- Nosil P. Transition rates between specialization and generalization in phytophagous insects. Evolution. 2002;56:1701–1706. doi: 10.1111/j.0014-3820.2002.tb01482.x. [DOI] [PubMed] [Google Scholar]
- Pearse IS, Altermatt F. Predicting novel trophic interactions in a non-native world. Ecol Lett. 2013;16:1088–1094. doi: 10.1111/ele.12143. [DOI] [PubMed] [Google Scholar]
- Pellmyr O, Leebens Mack J, Thompson JN. Herbivores and molecular clocks as tools in plant biogeography. Biol J Linnean Soc. 1998;63:367–378. [Google Scholar]
- Percy DM, Page RD, Cronk QC. Plant–insect interactions: double-dating associated insect and plant lineages reveals asynchronous radiations. Syst Biol. 2004;53:120–127. doi: 10.1080/10635150490264996. [DOI] [PubMed] [Google Scholar]
- Prince LM, Kress WJ. Phylogenetic relationships and classification in Marantaceae: insights from plastid DNA sequence data. Taxon. 2006;55:281–296. [Google Scholar]
- R-Development-Core-Team. R: a language and environment for statistical computing 2.10.1. R Foundation for Statistical Computing; Vienna, Austria: 2009. http://www.R-project.org. [Google Scholar]
- Raven PH, Axelrod DI. Angiosperm biogeography and past continental movements. Ann Mo Bot Gard. 1974;61:539–673. [Google Scholar]
- Saul WC, Jeschke JM. Ecoevolutionary experience in novel species interactions. Ecol Lett. 2015;18:236–245. doi: 10.1111/ele.12408. [DOI] [PubMed] [Google Scholar]
- Specht CD, Kress WJ, Stevenson DW, DeSalle R. A molecular phylogeny of Costaceae (Zingiberales) (vol 21, pg 333, 2001) Mol Phylogenet Evol. 2002;21:333–345. doi: 10.1006/mpev.2001.1029. (Errata 323, 395) [DOI] [PubMed] [Google Scholar]
- Staines CL, Garcia-Robledo C. The genus Cephaloleia Chevrolat, 1836 (Coleoptera, Chrysomelidae, Cassidinae) Zookeys. 2014;436:1–355. doi: 10.3897/zookeys.436.5766. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Strauss SY, Lau JA, Carroll SP. Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett. 2006;9:357–374. doi: 10.1111/j.1461-0248.2005.00874.x. [DOI] [PubMed] [Google Scholar]
- Strong DR. Rapid asymptotic species accumulation in phytophagous insect communities - pests of cacao. Science. 1974;185:1064–1066. doi: 10.1126/science.185.4156.1064. [DOI] [PubMed] [Google Scholar]
- Strong DR. Biogeographic dynamics of insect-host plant communities. Annu Rev Entomol. 1979;24:89–119. [Google Scholar]
- Suchan T, Alvarez N. Fifty years after Ehrlich and Raven, is there support for plant–insect coevolution as a major driver of species diversification? Entomol Exp Appl. 2015;157:98–112. [Google Scholar]
- Verhoeven KJ, Biere A, Harvey JA, Van Der Putten WH. Plant invaders and their novel natural enemies: who is naive? Ecol Lett. 2009;12:107–117. doi: 10.1111/j.1461-0248.2008.01248.x. [DOI] [PubMed] [Google Scholar]
- Wilf P, Labandeira CC, Kress WJ, Staines CL, Windsor DM, Allen AL, Johnson KR. Timing the radiations of leaf beetles: Hispines on gingers from latest Cretaceous to recent. Science. 2000;289:291–294. doi: 10.1126/science.289.5477.291. [DOI] [PubMed] [Google Scholar]
- Zar JH. Biostatistical analysis. 4. New Jersey, USA: 1999. p. 929. [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.





