Allochronic speciation, secondary contact, and reproductive character displacement in periodical cicadas (Hemiptera:<i>Magicicada</i>spp.): genetic, morphological, and behavioural evidence

Cooley, John R.; Simon, Chris; Marshall, David C.; Slon, Karen; Ehrhardt, Christopher J.

doi:10.1046/j.1365-294x.2001.01210.x

Cited by 69 publications

(78 citation statements)

References 38 publications

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“…Introgressive hybridization between M. septendecim and M. tredecim (23,24) has also been proposed to explain the origin of M. neotredecim. Our results corroborate the previously reported genetic closeness of M. neotredecim to M. septendecim and not to M. tredecim (15)(16)(17)(18), more consistent with the plasticity/ nurse-brood model (but see ref. 25 for the theoretical possibility of the introgressive hybridization model).…”

Section: Resultssupporting

confidence: 93%

“…To test these hypotheses, phylogenetic information about the relationships of species, broods, and populations is essential. However, phylogenetic studies of Magicicada have been largely limited to the Decim group (6,(14)(15)(16)(17)(18), and only rough divergence times among species have been inferred (8, 10). Thus, a comprehensive molecular phylogeny covering all of the extant broods, their phylogeography, and divergence time has been lacking until now.…”

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confidence: 99%

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

Sota

Yamamoto

Cooley

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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101

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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...

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Section: Resultssupporting

confidence: 93%

mentioning

confidence: 99%

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

Sota

Yamamoto

Cooley

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

101

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“…A second mechanism for assortative mating is for different forms to become reproductively active at different times, reproducing in different years [124], at different times of the year [125], or at different times of the day [107,126]. This reduces the likelihood of interspecific mating and permits the continued coexistence of allochronic species.…”

Section: Discussionmentioning

confidence: 99%

Molecular Population Structure ofJunoniaButterflies from French Guiana, Guadeloupe, and Martinique

Gemmell

Borchers

Marcus

2014

Psyche: A Journal of Entomology

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Up to 9 described species of Junonia butterflies occur in the Americas, but authorities disagree due to species similarities, geographical and seasonal variability, and possible hybridization. In dispute is whether Caribbean Junonia are conspecific with South American species. Cytochrome oxidase I (COI) barcodes, wingless (wg) sequences, and Randomly Amplified Fingerprints (RAF) were studied to reveal Junonia population structure in French Guiana, Guadeloupe, Martinique, and Argentina. Phylogenetic analysis of COI recovered 2 haplotype groups, but most Junonia species can have either haplotype, so COI barcodes are ambiguous. Analysis of nuclear wingless alleles revealed geographic patterns but did not identify Junonia species. Nuclear RAF genotyping distinguished 11 populations of Junonia arranged into 3 clusters. Gene flow occurs within clusters but is limited between clusters. One cluster included all Argentinian samples. Two clusters included samples from French Guiana, Martinique, and Guadeloupe and appear to be divided by larval host plant use (Lamiales versus Scrophulariales). Many Junonia taxa were distributed across populations, possibly reflecting patterns of genetic exchange. We had difficulty distinguishing between the Caribbean forms J. zonalis and J. neildi, but we demonstrate that Caribbean Junonia are genetically distinct from South American J. evarete and J. genoveva, supporting the taxonomic hypothesis that they are heterospecific.

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“…Our model addresses the processes that select for prime-numbered life cycles, or the second part of the hybridization hypothesis. To address the first part of the hypothesis and to resolve conflicts between this hypothesis and other hypotheses for the evolution of periodical cicada life cycles (5,6,16,17), studies are needed on the genetic and environmental basis of periodicity.…”

Section: Discussionmentioning

confidence: 99%

“…cated in allowing periodical cicadas to switch life cycles (6,(16)(17)(18), and the phenomenon of off-cycle emergences, or ''straggling'' is also likely a manifestation of life cycle plasticity. Periodical cicada life cycle plasticity may itself be subject to evolutionary change (10), and we know little about the genetics of life cycle plasticity; thus, there is no simple way to include it in our models.…”

Section: S Ementioning

confidence: 99%

Allee effect in the selection for prime-numbered cycles in periodical cicadas

Tanaka

Yoshimura²,

Simon³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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Periodical cicadas are well known for their prime-numbered life cycles (17 and 13 years) and their mass periodical emergences. The origination and persistence of prime-numbered cycles are explained by the hybridization hypothesis on the basis of their lower likelihood of hybridization with other cycles. Recently, we showed by using an integer-based numerical model that prime-numbered cycles are indeed selected for among 10-to 20-year cycles. Here, we develop a real-number-based model to investigate the factors affecting the selection of prime-numbered cycles. We include an Allee effect in our model, such that a critical population size is set as an extinction threshold. We compare the real-number models with and without the Allee effect. The results show that in the presence of an Allee effect, prime-numbered life cycles are most likely to persist and to be selected under a wide range of extinction thresholds.extinction thresholds ͉ hybridization ͉ Magicicada ͉ predator satiation

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Allochronic speciation, secondary contact, and reproductive character displacement in periodical cicadas (Hemiptera:Magicicadaspp.): genetic, morphological, and behavioural evidence

Cited by 69 publications

References 38 publications

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

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

Molecular Population Structure ofJunoniaButterflies from French Guiana, Guadeloupe, and Martinique

Allee effect in the selection for prime-numbered cycles in periodical cicadas

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