Independent divergence of 13- and 17-y life cycles among three periodical cicada lineages

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.life-cycle shift | nurse brood | parallel evolution | speciation P eriodical cicadas (Magicicada) in the eastern United States represent one of the most spectacular life history and population phenomena in nature (1-10). These periodical cicadas spend most of their lives (13 y in the south, 17 y in the north) as underground juveniles except for a brief 2-to 4-wk period when adults emerge simultaneously in massive numbers. With few exceptions, at any given location, all of the periodical cicadas share the same life cycle and emerge on the same schedule, forming a single-year class referred to as a "brood." Surprisingly, each brood consists of multiple species from three species groups (Decim, Cassini, Decula).These three groups were considered to have diverged from each other allopatrically and to have later become sympatric and formed 13-and 17-y life cycles (2). The prolonged, primenumbered life cycles were hypothesized to have evolved in response to Pleistocene climatic cooling (9, 11) to avoid the adverse effect of low population density on mating success (9, 12, 13). Another view hypothesized that the long synchronized life cycles evolved in association with the predator avoidance strategy (2,4,8) and that this took place before both the glacial periods and the split of the three species groups (10) based on approximate genetic distances among species groups (8). To test these hypotheses, phylogenetic information about the r...

Two sides of a coin: ecological and chronobiological perspectives of timing in the wild

“…In addition to circa-rhythms, which approximate geophysical time-scales, biological processes are organized by further internal rhythms with no counterparts in the environment [26]. These range from ultradian time-scales, exemplified above for voles, to multi-year rhythms, for example, in cicada [53]. Although conceptually distinct, these rstb.royalsocietypublishing.org Phil.…”

Molecular phylogenetics, diversification, and systematics of Tibicen Latreille 1825 and allied cicadas of the tribe Cryptotympanini, with three new genera and emphasis on species from the USA and Canada<br />(Hemiptera: Auchenorrhyncha: Cicadidae)

“…While the extraordinary periodical cicadas (Magicicada Davis, seven spp.) have been extensively studied for nearly two centuries, including molecular and morphological systematic analyses (Marlatt 1907;Simon 1979;1983;Sota et al 2013;Williams & Simon 1995), the 185 non-periodical species and subspecies north of Mexico have received only sporadic attention and little to no phylogenetic analysis beyond alpha taxonomy and a role as outgroups in other studies (e.g., Moulds 2005;Sueur et al 2007). …”

Regularities and irregularities in periodical cicada evolution

“…This congruence of geographic clades across species is one of the revelations of Sota et al (1) and suggests parallel evolution of the species constituting these clades. However, the congruence does not hold up in all cases.…”

“…Although Sota et al (1) have brought much clarification to our current understanding of Magicicada evolution, there remains a need for even deeper sampling of individuals and genes. What I have called "clades" are referred to as "haplotype groups" by Sota et al, because the mitochondrial trees (figure S1 in ref.…”

“…Sota et al (1) conclude that the "repeated shifts between the two prime-numbered life cycles in all three Magicicada species groups suggest a common genetic basis that evolved prior to the origin of the species groups," or in other words, that there is ancestral variation for life-cycle length. Identifying and locating such genes or gene regions would certainly carry us much further toward understanding Magicicada evolution.…”