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Convergent Evolution of 'Creepers' in the Hawaiian Honeycreeper

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Convergent Evolution of 'Creepers' in the Hawaiian Honeycreeper ARTICLE IN PRESS Biol. Lett. 1. INTRODUCTION doi:10.1098/rsbl.2008.0589 Adaptive radiation is a fascinating evolutionary pro- 1 cess that has generated much biodiversity. Although 65 2 Evolutionary biology several mechanisms may be responsible for such 66 3 diversification, the ‘ecological theory’ holds that it is 67 4 the outcome of divergent natural selection between 68 5 Convergent evolution of environments (Schluter 2000). Whether adaptive 69 6 radiations result chiefly from such ecological speciation, 70 7 ‘creepers’ in the Hawaiian however, remains unclear (Schluter 2001). Convergent 71 8 evolution is often considered powerful evidence for the 72 9 honeycreeper radiation role of adaptive forces in the speciation process 73 (Futuyma 1998), and thus documenting cases where it 10 Dawn M. Reding1,2,*, Jeffrey T. Foster1,3, 74 has occurred is important in understanding the link 11 Helen F. James4, H. Douglas Pratt5 75 12 between natural selection and adaptive radiation. 76 and Robert C. Fleischer1 13 The more than 50 species of Hawaiian honeycree- 77 1 14 Center for Conservation and Evolutionary Genetics, National pers (subfamily Drepanidinae) are a spectacular 78 Zoological Park and National Museum of Natural History, 15 Smithsonian Institution, Washington, DC 20008, USA example of adaptive radiation and an interesting 79 16 2Department of Zoology, University of Hawaii, Honolulu, system to test for convergence, which has been 80 17 HI 96822, USA suspected among the nuthatch-like ‘creeper’ eco- 81 3Center for Microbial Genetics & Genomics, Northern Arizona 18 morph on the islands (figure 1). The Hawaii creeper 82 University, Flagstaff, AZ 86011, USA 19 4Division of Birds, National Museum of Natural History, (Oreomystis mana) has traditionally been allied with 83 20 Washington, DC 20013, USA the Kauai creeper (Oreomystis bairdi ), either as con- 84 5 21 North Carolina State Museum of Natural Sciences, 11 West Jones specific (Amadon 1950) or as a congener (Henshaw 85 Street, Raleigh, NC 27601, USA 22 *Author and address for correspondence: Department of Ecology, 1902; Pratt 1992). The two birds share many 86 23 Evolution, and Organismal Biology, Iowa State University, similarities including bill shape, foraging and mob- 87 24 Ames, IA 50011, USA ([email protected]). bing behaviours, and juvenile plumage pattern (Pratt 88 25 Natural selection plays a fundamental role in the 1992; Foster et al. 2000; Lepson & Woodworth 89 26 ecological theory of adaptive radiation. A pre- 2001). Their juvenile begging calls are nearly identical 90 27 diction of this theory is the convergent evolution and distinct from those known for other honeycree- 91 28 of traits in lineages experiencing similar pers (Pratt 2001). Both species possess a narrow, 92 29 environments. The Hawaiian honeycreepers are simple notch-tipped tongue very different from the 93 30 a spectacular example of adaptive radiation tubular tongues of most other honeycreepers (Pratt 94 31 and may demonstrate convergence, but uncer- 1992), including akepas (Loxops) and amakihis (Hemi- 95 32 tainty about phylogenetic relationships within gnathus in part). But despite these apparent synapo- 96 the group has made it difficult to assess such 33 morphies, recent osteological and mitochondrial 97 evolutionary patterns. We examine the phyloge- 34 netic relationships of the Hawaii creeper DNA (mtDNA) evidence (Fleischer et al. 2001; 98 35 (Oreomystis mana), a bird that in a suite of James 2004) suggests these two species are evolution- 99 36 morphological, ecological and behavioural arily quite distant, and instead points to a close 100 37 traits closely resembles the Kauai creeper relationship between O. mana and the cross-billed 101 38 (Oreomystis bairdi ), but whose mitochondrial akepas or curve-billed amakihis. Pratt (2001) 102 39 DNA (mtDNA) and osteology suggest a relation- remarked that if the Kauai and Hawaii creepers 103 40 ship with the amakihis (Hemignathus in part) derived their diverse similarities by convergence, they 104 41 and akepas (Loxops). We analysed nuclear DNA would present the most dramatic example of conver- 105 42 sequence data from 11 relevant honeycreeper gent evolution yet discovered in birds. 106 taxa and one outgroup to test whether the 43 As an alternative explanation for the conflicting 107 character contradiction results from historical 44 hybridization and mtDNA introgression, or con- phylogenetic evidence, Pratt (2001) suggested a past 108 45 Q1 vergent evolution. We found no evidence of past hybridization event. Under this scenario, hybrids 109 46 hybridization, a phenomenon that remains would have involved male Oreomystis mating with 110 47 undocumented in Hawaiian honeycreepers, and female akepa or amakihi. If the Hawaii creeper 111 48 confirmed mtDNA and osteological evidence descended from such offspring, it could have retained 112 49 that the Hawaii creeper is the most closely most of the phenotypic characteristics of Oreomystis 113 50 related species to the amakihis and akepas. but possess mtDNA from the introgressing species. 114 51 Thus, the morphological, ecological and beha- Hybridization can result in a significantly different 115 52 vioural similarities between the evolutionarily genealogy for mtDNA from that of most genes in a 116 distant Hawaii and Kauai creepers represent an 53 species, as mtDNA is more likely to introgress than 117 extreme example of convergent evolution and 54 demonstrate how natural selection can lead to nuclear DNA (nucDNA; Ballard & Whitlock 2004). 118 55 repeatable evolutionary outcomes. Indeed, mtDNA from one taxon can completely replace 119 56 that in another, with little or no evidence of nuclear 120 57 Keywords: ecological convergence; introgression or morphological change (Bernatchez 121 58 convergent evolution; Hawaiian honeycreepers; et al.1995). No unequivocal cases of hybridization have 122 59 mitochondrial DNA introgression; hybridization; yetbeendocumentedinHawaiianhoneycreepers.If 123 60 adaptive radiation past introgression is responsible for the incongruence 124 61 between mitochondrial sequences and some striking 125 62 phenotypic characters, nucDNA markers should reveal 126 63 Electronic supplementary material is available at http://dx.doi.org/ the contribution of the Oreomystis lineage to the genetic 127 64 10.1098/rsbl.2008.0589 or via http://journals.royalsociety.org. signal of the Hawaii creeper. 128 Received 20 October 2008 Accepted 26 November 2008 1 This journal is q 2008 The Royal Society RSBL 20080589—5/12/2008—16:41—CHANDRAN—318457—XML – pp. 1–5 ARTICLE IN PRESS 2 D. M. Reding et al. Convergence in Hawaiian honeycreepers 129 193 (a) (b) 130 194 131 195 132 196 133 197 134 198 135 199 136 200 137 201 138 202 139 203 140 204 141 205 142 206 143 207 144 208 145 Figure 1. Photographic comparison of the (a) Kauai creeper and (b) Hawaii creeper. Photographs by Jack Jeffrey. 209 146 210 147 Here, we examine nucDNA sequences from several for placement of Hawaii creeper with the akepas and 211 148 honeycreeper species to test whether convergence or amakihis, as noted by a high posterior probability 212 149 introgression characterizes the relationship between value of 1.0 for this clade (figure 2). Trees con- 213 150 the Hawaii and Kauai creepers. structed using mtDNA sequences from the specimens 214 151 in this analysis (figure S3, in the electronic supple- 215 152 mentary material) were nearly identical to the trees 216 2. MATERIAL AND METHODS 153 from the nuclear gene analyses (figure 2)and 217 We analysed 19 individuals belonging to 11 relevant honeycreeper 154 taxa and one outgroup. See appendix S1, electronic supplementary generally matched previous trees based on more taxa, 218 155 material, for provenance of samples. Five distinct gene regions, especially with regards to the position of the Hawaii 219 156 including four nuclear introns and one exon (see electronic creeper (Fleischer et al. 2001). 220 supplementary material), generated ca 2500 BP of sequence data. 157 We analysed the intron and exon datasets both separately and Constraining the topology such that the Hawaii 221 158 concatenated. We conducted a homogeneity partition test (ILD, and Kauai creepers formed a monophyletic group 222 159 Farris et al. 1995) with heuristic search, as implemented in the increased the length of the MP tree by eight steps and 223 program PAUPÃ v. 4.0.b10 (Swofford 2002), to evaluate the 160 lowered the score of the ML tree by 28.6. Likelihood 224 congruence of phylogenetic signal between the two sequence sets. 161 We reconstructed phylogenies using three approaches: maximum scores of the constrained trees were significantly 225 162 parsimony (MP); maximum likelihood (ML); and Bayesian infer- worse ( pZ0.007, S–H test) than that of figure 2. 226 163 ence (see electronic supplementary material). To evaluate the 227 strength of the evidence for the placement of the Hawaii creeper 164 with akepa/amakihi versus Kauai creeper, we subsequently applied 228 165 constraints in the MP and ML methods to force the alternative 4. DISCUSSION 229 166 topology, and compared the resulting ML trees with the uncon- By corroborating the phylogeny obtained from 230 strained trees using the S–H test (Shimodaira & Hasegawa 1999; 167 231 see electronic supplementary material). In addition to the nucDNA mtDNA and osteology, the results from nucDNA 168 data, we obtained and analysed 1254 bp of mtDNA sequences from markers indicate that creepers in the Hawaiian Islands 232 169 the same specimens (see electronic supplementary material for
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