Regularities and irregularities in periodical cicada evolution.

Periodical cicadas are one of those creatures that everyone in eastern North America knows, if only periodically. The seemingly magical invasion every 17 or 13 y of millions upon millions of black, red-eyed, vaguely demonic-looking insects that fill the air with their incessant droning is, indeed, not something that one can easily ignore. These insects even inspired Bob Dylan, in his song “Day of the Locusts,” to proclaim that the cicadas were singing just for him, which seems at odds with current evolutionary theory. In PNAS, Sota et al. (1) make a much more meaningful contribution to our understanding of the evolution of the genus Magicicada. Evolutionary interest in periodical cicadas is driven by their singular life history. The basic life cycle, with a long nymphal stage that feeds underground on the roots of trees and then emerges into a brief adult stage, which mates and oviposits, is not in itself unusual. But they have not only the longest total life cycle of any insect, but two alternative long cycles of 13 and 17 y. The fact that 13 and 17 are prime numbers has not escaped the attention of evolutionary theorists (the literature of Magicicada may be unique in encompassing both pest management and mathematical journals; see for example, ref. 2). However, the peculiarities do not stop there. Each species is organized into several developmentally synchronized “broods” (15 total across all species), each with its own characteristic years of adult emergence and geographic range. However, here is the real kicker: almost all broods contain three morphologically distinct, rarely interbreeding forms, called Decula, Cassini, and Decim, all of which have life cycles synchronized with each other. Note that I intentionally used the nonspecific term “forms” in the preceding sentence. This is because species concepts for these insects have been fluid. The morphologically distinct Decula, Cassini, and Decim are species under any conceivable concept, but current opinion (3) is to consider these as species groups and set the species category one level lower, treating the morphologically identical and genetically very similar 17and 13-y populations in each species group as operational species (e.g., 17-y Magicicada septendecula and 13-y Magicicada tredecula of group Decula) for a total of six species. (The symmetry of this system was upset by the recent identification of Magicicada neotredecim, about which more later.) All broods of each of these species have occasionally been proposed as species. Sota et al. (1) have now uniquely cast a great deal of light on the Magicicada species problem by providing a phylogeny that includes all species groups, species, and broods. However, in doing so they also add a whole new level of complexity, consisting of significant geographic population structure within each species group, based originally on mitochondrial sequences and now reinforced by nuclear sequences. The pattern in Decim (4) consists of four geographic clades: eastern, middle, and western in the northern half of eastern North America, and the B clade in the southern half. However, the remarkable part of this division is that this phylogeographic pattern is now seen to be repeated in the Cassini and Decula species groups, with the exception that they lack the B clade. The capstone to this parallel population structure is the inclusion across the three species groups of the same clades in a given brood. If you are confused at this point, you are not alone; I had to ponder all this for quite some time before I could begin writing this commentary. To assist in explaining the fresh insights of Sota et al. (1), I combined elements of their figures 1 and 2 (figures 1 and 2 in ref. 1) and made some simplifications (see the legend to Fig. 1 for species name abbreviations). To understand Fig. 1, imagine that you are in New Jersey later this very year and visit a local wood, aswarm with millions, if not billions, of cicadas. You pick one from your shirt and study it carefully. By going to www.magicicada.org on your cell phone you discover that only brood II is emerging in this area this year. Using the instant DNA sequencing application of your cell phone that will no doubt soon be available, you obtain a mitochondrial sequence that matches sequences from a 17-y, eastern mitochondrial clade containing Magicicada cassini (Cas17 in Fig. 1). Traveling further down the tree in Fig. 1 tells us it is from the species group Cassini. We then sample a few more cicadas, and find not only other M. cassini sequences, but Fig. 1. (A) Female of the 17-y periodical cicada M. septendecim laying eggs in a twig. Image reproduced from ref. 9. (B) Simplified schematic of the phylogeny of Magicicada showing relationships of species groups, geographic clades, species, and broods. Branch lengths not to scale. Species are abbreviated by denoting Decula, Cassini, and Decim as Dec, Cas, and Dcm, respectively, and replacing the prefixes Septen and Tredec with the suffixes 17 and 13, respectively. Thus, M. septemdecim is abbreviated Dcm17. M. neotredecim is abbreviated NeoDcm13. See text for full explanation. B+ means that the Decim B clade plus other clades of Decula and Cassini occur in this area.