Reproductive Character Displacement and Speciation in Periodical Cicadas, With Description of a New Species, 13-Year Magicicada Neotredecim

Self Cite

101

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...

Section: Resultsmentioning

confidence: 99%

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

Sota

Yamamoto

Cooley

et al. 2013

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101

“…Several factors may cause reproductive isolation among sympatric populations, including a host shift (15), a change in breeding time (16), and infection with CI inducers (3,8). Nasonia parasitoid wasps have three sibling species (Nasonia vitripennis, Nasonia longicornis, and Nasonia giraulti) and show bidirectional CI among the species, caused by different strains of Wolbachia (17,18).…”

Section: Discussionmentioning

confidence: 99%

Unique clade of alphaproteobacterial endosymbionts induces complete cytoplasmic incompatibility in the coconut beetle

Takano

Tuda

Takasu

et al. 2017

Maternally inherited bacterial endosymbionts in arthropods manipulate host reproduction to increase the fitness of infected females. Cytoplasmic incompatibility (CI) is one such manipulation, in which uninfected females produce few or no offspring when they mate with infected males. To date, two bacterial endosymbionts, Wolbachia and Cardinium, have been reported as CI inducers. Only Wolbachia induces complete CI, which causes 100% offspring mortality in incompatible crosses. Here we report a third CI inducer that belongs to a unique clade of Alphaproteobacteria detected within the coconut beetle, Brontispa longissima. This beetle comprises two cryptic species, the Asian clade and the Pacific clade, which show incompatibility in hybrid crosses. Different bacterial endosymbionts, a unique clade of Alphaproteobacteria in the Pacific clade and Wolbachia in the Asian clade, induced bidirectional CI between hosts. The former induced complete CI (100% mortality), whereas the latter induced partial CI (70% mortality). Illumina MiSeq sequencing and denaturing gradient gel electrophoresis patterns showed that the predominant bacterium detected in the Pacific clade of B. longissima was this unique clade of Alphaproteobacteria alone, indicating that this endosymbiont was responsible for the complete CI. Sex distortion did not occur in any of the tested crosses. The 1,160 bp of 16S rRNA gene sequence obtained for this endosymbiont had only 89.3% identity with that of Wolbachia, indicating that it can be recognized as a distinct species. We discuss the potential use of this bacterium as a biological control agent.

“…Replicate speciation has produced three parallel species pairs of 13-and 17-year periodical cicadas (Magicicada species), with one of the 17-year populations (M. septendecim) giving rise to a 13-year species (M. neotredecim), forming a species pair (septendecim-neotredecim) within a species pair (tredecimseptendecim) (34). The recurrent phylogenetically abrupt switches between these two life cycles suggests that, as in the replicate species pairs of fishes, some ancestral developmental mechanism with a 4-year periodicity has repeatedly influenced life-cycle divergence between the species pairs of periodical cicadas (5,35), although the physiological mechanism is poorly understood.…”

Section: Developmental Recombination and Parallel Species Pairsmentioning

confidence: 99%

Developmental plasticity and the origin of species differences

West‐Eberhard

2005

810

661

Speciation is the origin of reproductive isolation and divergence between populations, according to the ''biological species concept'' of Mayr. Studies of reproductive isolation have dominated research on speciation, leaving the origin of species differences relatively poorly understood. Here, I argue that the origin of species differences, and of novel phenotypes in general, involves the reorganization of ancestral phenotypes (developmental recombination) followed by the genetic accommodation of change. Because selection acts on phenotypes, not directly on genotypes or genes, novel traits can originate by environmental induction as well as mutation, then undergo selection and genetic accommodation fueled by standing genetic variation or by subsequent mutation and genetic recombination. Insofar as phenotypic novelties arise from adaptive developmental plasticity, they are not ''random'' variants, because their initial form reflects adaptive responses with an evolutionary history, even though they are initiated by mutations or novel environmental factors that are random with respect to (future) adaptation. Change in trait frequency involves genetic accommodation of the threshold or liability for expression of a novel trait, a process that follows rather than directs phenotypic change. Contrary to common belief, environmentally initiated novelties may have greater evolutionary potential than mutationally induced ones. Thus, genes are probably more often followers than leaders in evolutionary change. Species differences can originate before reproductive isolation and contribute to the process of speciation itself. Therefore, the genetics of speciation can profit from studies of changes in gene expression as well as changes in gene frequency and genetic isolation.speciation ͉ genetic accommodation ͉ adaptive evolution ͉ novelty ͉ parallel evolution