Founder Effects Initiated Rapid Species Radiation in Hawaiian Cave Planthoppers
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Founder effects initiated rapid species radiation in Hawaiian cave planthoppers Andreas Wessela,1, Hannelore Hocha, Manfred Aschea, Thomas von Rintelena, Björn Stelbrinka, Volker Heckb, Fred D. Stonec, and Francis G. Howarthd aDepartment of Research, Museum für Naturkunde – Leibniz-Institut für Evolutions-und Biodiversitätsforschung an der Humboldt-Universität zu Berlin, D-10115 Berlin, Germany; bGeography, Department of Physics, University of Siegen, D-57068 Siegen, Germany; cMath and Natural Sciences Department, Hawai‘i Community College, Hilo, HI 96720-4091; and dDepartment of Natural Science, Bishop Museum, Honolulu, HI 96817 Edited by Francisco J. Ayala, University of California, Irvine, CA, and approved April 25, 2013 (received for review January 25, 2013) The Hawaiian Islands provide the venue of one of nature’sgrand a unique subterranean environment consisting of interconnected experiments in evolution. Here, we present morphological, behav- systems of air-filled voids of varying sizes up to lava tube caves that ioral, genetic, and geologic data from a young subterranean insect can extend up to several dozen kilometers. These subterranean lineage in lava tube caves on Hawai‘i Island. The Oliarus polyphe- voids host diverse root communities (12–14), with food webs mus species complex has the potential to become a model for largely sustained by living roots of the pioneer plant Metrosideros studying rapid speciation by stochastic events. All species in this polymorpha (Myrtaceae) (SI Appendix,Fig.S1). Roots are ephem- lineage live in extremely similar environments but show strong eral resources, because their abundance decreases with increasing differentiation in behavioral and morphometric characters, which cave age through ecological succession on the surface (SI Appendix, are random with respect to cave age and geographic distribution. Text S2). Our observation that phenotypic variability within populations Species of Oliarus are the only obligatory cave-dwelling pri- decreases with increasing cave age challenges traditional views mary consumers in this ecosystem (15). The Hawaiian Oliarus on founder effects. Furthermore, these cave populations are natu- (Nesoliarus) clade is a monophyletic endemic radiation (16) ral replicates that can be used to test the contradictory hypotheses. comprising about 85 known species. The latter include seven Moreover, Hawaiian cave planthoppers exhibit one of the highest exclusively cave-dwelling species that have been described to EVOLUTION speciation rates among animals and, thus, radically shift our per- date from three islands (17). Three cave taxa are endemic to ception on the evolutionary potential of obligate cavernicoles. Hawai‘i Island, but only O. polyphemus is widely distributed, inhabiting lava tubes on all major volcanoes except Kohala. The density-dependent selection | dynamic adaptive landscape | nonadaptive inhabited caves occur from sea level to about 2,000 m and range speciation | sexual behavior | vibrational communication in age from less than 50 to several thousand years (18) (Fig. 1 and SI Appendix,Fig.S3). O. polyphemus exhibits extreme character he role of extrinsic factors such as environmental changes in reduction (eyes, wings, pigmentation) associated with its trog- Tdriving genetic change in populations is largely undisputed. lobitic habit (SI Appendix,Fig.S2). Genetic drift (i.e., random changes in gene frequency attributable Given the extreme degree of troglomorphy in O. polyphemus, to stochastic allele assortment) also affects all populations, but its dispersal is only possible by subterranean migration, which is con- fi role in yielding signi cant differences between populations in strained by the patchy distribution of resources, both at the intra- interplay with selective forces is controversially discussed. Ge- lava tube (root patches within lava tubes) and interlava tube (and netic drift is most effective in small populations, the best-known lava flow) levels. A certain level of migration is necessary to examples being drastic population bottlenecks or founding indi- maintain populations despite the risk of extinction through eco- viduals (e.g., during the colonization of islands). These observa- logical succession or catastrophic events (see SI Appendix, Text S2 tions led to the development of the much-debated founder-effect for a discussion of modes of subterranean migration). The high concept by Mayr (1). This concept was further developed by in- level of phenotypic and genetic differentiation found between cluding population structure and sexual selection (2, 3) but has – geographically proximate, young caves suggests largely isolated remained contentious (4 6) (for reviews, see refs. 7 and 8). Here, populations and low migration rate through rare and accidental we revisit the founder-effect concepts using the blind plan- Oliarus polyphemus dispersal. This essentially implies a series of many founder events in thopper in the Hawaiian lava tube caves as the establishment of new populations (SI Appendix,Fig.S8and a model system. The Hawaiian cave planthopper system provides Text S2). If the migration rate is low, each new cave population excellent opportunities to test models of stochastic effects in would be descended from a single or few founding events from evolution in a natural setting, because it is simple enough for fl neighboring older established populations. Because even young distinguishing the in uence of many of the major factors involved caves have established populations (SI Appendix,TableS5), the and encompasses natural populations undergoing repeated “ ” age of the founding event probably approximates the age of the events (replicates of natural experiments ) under similar con- lava flow. The minimum speed of dispersal has been estimated ditions where many of the relevant biotic and abiotic factors can at >10 m/y (SI Appendix, Text S2), which is compatible with the be assessed. Grounds and Habits of the Hawaiian Cave Planthoppers Author contributions: A.W., H.H., and F.G.H. designed research; A.W., H.H., M.A., B.S., The Hawaiian archipelago, the most remote group of high islands F.D.S., and F.G.H. performed research; V.H. contributed new reagents/analytic tools; A.W., in the world, hosts a highly diverse endemic fauna. Much of this T.v.R., B.S., and V.H. analyzed data; and A.W. wrote the paper. diversity is the result of radiations following rare colonization The authors declare no conflict of interest. events on the islands (9). The Hawaiian chain was formed by This article is a PNAS Direct Submission. “ ” outpourings of lava from a volcanic hot spot (10), and volcanoes Data deposition: The data reported in this paper have been deposited in the European are still active on its youngest and largest island, Hawai‘i. This Nucleotide Archive (ENA), www.ebi.ac.uk/ena (accession nos. HF674815–HF674838). active volcanism causes rapid landscape dynamics [e.g., 90% of the 1To whom correspondence should be addressed. E-mail: [email protected]. entire surface area of Kllauea Volcano has been replaced within This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. the past 1,500 y (11)]. The nearly continuous flow of lava creates 1073/pnas.1301657110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1301657110 PNAS Early Edition | 1of6 Downloaded by guest on September 25, 2021 A sp.1 Results fi sp. 2 Phenotypic Differentiation. Signi cant intercave differences in call patterns were observed in all 10 parameters measured for 12 populations (Fig. 1C and SI Appendix, Fig. S5 and Table S7). The significant differentiation found even between caves in close proximity indicates an interruption of gene flow between these caves. In “Pink Pistillaria,” two completely different call patterns were found (SI Appendix, Fig. S6), which, along with morpho- metric differences, indicate the coexistence of two sympatric species in the oldest (5,000–8,000 y) cave system known to har- bor cave planthoppers (SI Appendix, Table S5). Moreover, in one of the two Pink Pistillaria populations and in the “Kaumana” population, variation of some call parameters did not overlap with these parameters in all other populations studied (SI Ap- Mesonotum width pendix, Fig. S5). The population from “McKenzie Park” even Wing width Wing length showed a unique song structure with a regularly alternating duet, Length of rear tibia Relative wing length again suggesting the existence of a distinct species. Remarkably, McKenzie Park and Kaumana are among the youngest caves [i.e., formed after 1790 (SI Appendix, Fig. S3 and Table S5)]. B Similarly, significant morphometric differentiation between 18 cave populations was found in all 14 parameters measured, albeit to a lesser degree, because no gaps in the ranges of character variation were observed (SI Appendix, Table S7). A discriminant analysis including both song and morphometric parameters variance revealed a 100% assignment for 15 populations in at least one sex for at least one character complex (SI Appendix, Table S8). Historical time (after 1790) The differences between populations do not follow a pattern of 200-750 B.P. clinal variation in either call patterns or morphology (Fig. 1A). In 012345 750-1,500 B.P. addition, no correlation between the degree of morphological cave age [ka] 5,000-10,000 B.P. differentiation and cave age was found. Interestingly, the only C correlation found is a negative one of phenotypic character variability to cave age; this correlation is significant or highly