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, 110 (17), 6919-24

Independent Divergence of 13- And 17-y Life Cycles Among Three Periodical Cicada Lineages

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Independent Divergence of 13- And 17-y Life Cycles Among Three Periodical Cicada Lineages

Teiji Sota et al. Proc Natl Acad Sci U S A.

Abstract

The evolution of 13- and 17-y periodical cicadas (Magicicada) is enigmatic because at any given location, up to three distinct species groups (Decim, Cassini, Decula) with synchronized life cycles are involved. Each species group is divided into one 13- and one 17-y species with the exception of the Decim group, which contains two 13-y species-13-y species are Magicicada tredecim, Magicicada neotredecim, Magicicada tredecassini, and Magicicada tredecula; and 17-y species are Magicicada septendecim, Magicicada cassini, and Magicicada septendecula. Here we show that the divergence leading to the present 13- and 17-y populations differs considerably among the species groups despite the fact that each group exhibits strikingly similar phylogeographic patterning. The earliest divergence of extant lineages occurred ∼4 Mya with one branch forming the Decim species group and the other subsequently splitting 2.5 Mya to form the Cassini and Decula species groups. The earliest split of extant lineages into 13- and 17-y life cycles occurred in the Decim lineage 0.5 Mya. All three species groups experienced at least one episode of life cycle divergence since the last glacial maximum. We hypothesize that despite independent origins, the three species groups achieved their current overlapping distributions because life-cycle synchronization of invading congeners to a dominant resident population enabled escape from predation and population persistence. The repeated life-cycle divergences supported by our data suggest the presence of a common genetic basis for the two life cycles in the three species groups.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Phylogeny and divergence times of Magicicada resulting from a Bayesian relaxed clock analysis with nuclear and mitochondrial data showing different histories of divergence into 13- and 17-y species among the three species groups. Outgroup taxa are not shown. Bars show 95% highest probability density (HPD) intervals of estimated divergence times. For major nodes, divergence times and 95% HPD intervals in brackets are described. Node supports are posterior probabilities of the Bayesian inference and bootstrap percentages in a maximum-likelihood analysis (shown when >0.70 or >70%). The label for each OTU describes the sample code (Table S1), species, and brood number. Mitochondrial haplotype groups (Fig. 2) of samples are also shown.
Fig. 2.
Fig. 2.
Mitochondrial haplotype networks for each species group (A–C) showing different patterns of haplotype sharing between 13- and 17-y species. Each circle represents a unique haplotype, where size is proportional to sample size. Lines represent 1-bp differences, and open circles represent missing haplotypes not appearing in the samples. The composition (relative sample sizes) of broods is shown as a pie chart, in which broods are distinguished by different colors. (D–F) Geographic distribution of haplotype groups (distinguished by the color of the circle) in each species group showing similar phylogeographic divisions. Brood numbers are indicated by Arabic numerals beside the circles. Dotted lines indicate the boundary of 13- and 17-y life cycles. Colors in A–C do not correspond to colors in D–F.
Fig. 3.
Fig. 3.
Differentiation in AFLP loci among groups defined by life cycle and mitochondrial haplotype group (geographic region). The relationships among groups are depicted by the unrooted neighbor-joining tree based on pairwise Nei’s distances. Node supports are bootstrap percentages (shown when >50%). Pairwise Fst and P values among groups in each species group are given in inset tables. Fst values in bold letters are significant at α = 0.05 after controlling for the false-positive rate.
Fig. 4.
Fig. 4.
Divergence times between 17- and 13-y cicadas in three groups inferred by the isolation-with-migration approach. (A) Between M. septendecim and M. neotredecim in Decim Aw. (B) Between M. cassini and M. tredecassini in Cassini Cw. (C) Between M. tredecula and M. septendecula in Decula.
Fig. 5.
Fig. 5.
BSPs showing demographic histories of the three Magicicada species groups, Decim (A), Cassini (B), and Decula (C), based on mitochondrial gene sequence data. Thick solid curves indicate mean effective population sizes, and gray areas the 95% HPD limits. Dotted lines indicate the beginning of the Holocene (elevated air temperatures).

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