Life Cycle Replacement by Gene Introduction under an Allee Effect in Periodical Cicadas

et al. (2011) Life Cycle Replacement by Gene Introduction under an Allee Effect in Periodical Cicadas. PLoS ONE 6(4): e18347. doi:10.1371/journal.pone.0018347 Life Cycle Replacement by Gene Introduction under an Allee Effect in Periodical Cicadas Yukiko Nariai 0 Saki Hayashi 0 Satoru Morita 0 Yoshitaka Umemura 0 Kei-ichi Tainaka 0 Teiji Sota 0 John R. Cooley 0 Jin Yoshimura 0 Matjaz Perc, University of Maribor, Slovenia 0 1 Department of Systems Engineering, Shizuoka University , Hamamatsu , Japan , 2 Faculty of Information Science, Shizuoka University , Hamamatsu , Japan , 3 Department of Zoology, Kyoto University , Kyoto , Japan , 4 Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, Connecticut, United States of America, 5 Marine Biosystems Research Center, Chiba University , Kamogawa, Chiba , Japan , 6 Department of Environmental and Forest Biology, State University of New York College of Environmental Science and Forestry , Syracuse, New York , United States of America Periodical cicadas (Magicicada spp.) in the USA are divided into three species groups (-decim, -cassini, -decula) of similar but distinct morphology and behavior. Each group contains at least one species with a 17-year life cycle and one with a 13-year cycle; each species is most closely related to one with the other cycle. One explanation for the apparent polyphyly of 13and 17-year life cycles is that populations switch between the two cycles. Using a numerical model, we test the general feasibility of life cycle switching by the introduction of alleles for one cycle into populations of the other cycle. Our results suggest that fitness reductions at low population densities of mating individuals (the Allee effect) could play a role in life cycle switching. In our model, if the 13-year cycle is genetically dominant, a 17-year cycle population will switch to a 13-year cycle given the introduction of a few 13-year cycle alleles under a moderate Allee effect. We also show that under a weak Allee effect, different year-classes (''broods'') with 17-year life cycles can be generated. Remarkably, the outcomes of our models depend only on the dominance relationships of the cycle alleles, irrespective of any fitness advantages. - Funding: This work was supported in part by grants-in-aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan to J. Y. (nos. 22255004 and 22370010) and K. T. (20500204), a research grant from Ryozo Yamada Funds to J. Y. and J. R. C. acknowledge support from National Science Foundation DEB04-22386, DEB05-29679, DEB07-20664, and DEB07-22101 to Chris Simon. No additional external funding received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Cicadas are remarkable singing insects in tropical and temperate forests that belongs to family Cicadidae (Suborder: Homoptera; Order: Heteroptera) [1,2]. Male cicadas sing mating calls, while females are attracted to male calls [3,4]. Recently females are found to respond to males by wing flicking and mating proceeds with male-female communications [5]. Cicadas are also unique in their long juvenile stages in soil spreading 310 years and very short adult lives (a couple weeks), due to their feeding on poor-nutrient xylem water in tree roots [1,2,6]. In a short adult stage, females mate with males and lay eggs on small twigs, from where nymphs hatch soon or later and drop to the ground, and dig into the soil, where they feed on plant roots [7]. Periodical cicadas (Magicicada spp.) in the USA are unusual with excessively long prime-numbered life cycles of 13- or 17-years [812,6]. Among all cicadas, they are the only known group with periodicity [cite]. The known maturation determinant of all other cicadas is not time, but cumulative temperature [cite]. Periocical cicadas are also unique in their life histories, characterized by mass, synchronized emergences of millions per acre [13] and are divided into regional populations sharing emergence years (yearclasses, specifically called broods). Three taxonomic groups (-decim, -cassini, and -decula) contain 7 species. The -cassini and decula groups contain two species: 17-year M. cassini and 13-year M. tredecassini and 17-year M. septendecula and 13-year M. tredecula, respectively. The -decim group consists of three species: 17-year M. septendecim and 13-year M. tredecim and M. neotredecim. Each species is most closely related to one with the other life cycle in its own species group [11,14], and permanent life cycle shifts have been proposed to explain these relationships [11,1416]. The evolutionary origin of M. neotredecim appears to be a permanent life cycle shift from a 17-year to a13-year cycle. Genetic, behavioral, and biogeographic evidence suggest that M. neotredecim originated recently from the 17-year species M. septendecim [1417]. M. neotredecim is indistinguishable from 17-year M. septendecim genetically and morphologically, and it shows a striking pattern of reproductive character displacement in calling song pitch with the closely related species M. tredecim [14,16]. Within 17-year periodical cicadas, brood formation appears to occur via temporary life cycle shifts, in which large numbers of cicadas emerge off-cycle, perhaps in response to climate fluctuations (brood shifting) [11,18]. Among 17-year broods of periodical cicadas, differences of 61 or 64 years appear to be especially common [19 23]. Permanent life cycle switching involving small numbers of cicadas is difficult to explain, because small numbers of periodical cicadas may fail to reproduce [24] or be quickly destroyed by predators since Magicicada rely on predator satiation by extreme abundance [11,19,25 27]. Thus, any explanation for life cycle switching in periodical cicadas must take into account Allee Effects acting against small populations or minority life cycle phenotypes [28]. Here we investigate the possibility that life cycle switching between 13- and 17-year cycles can be explained by the introduction of a few life cycle alleles (individuals) into an isolated population with the other cycle. We construct a simple numerical model of hybridization between 17-year and 13-year cycles. Although hybridization and introgression in hybrid zones [2931] have been proposed as one factor stimulating permanent life cycle change in periodical cicadas [3235], our model of gene introduction is not genetic introgression in the strict sense, because there are no hybrid zones involved. In our model life cycle is assumed to be controlled by alleles at a locus under simple Mendelian inheritance, with one cycle (either 17- or 13-year) dominant to the other. Neither allele has a selective advantage except the advantage inherent in a shorter life cycle (generation time). We also consider diploid (...truncated)