John R. Cooley

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

Periodical cicadas have proven useful in testing a variety of ecological and evolutionary hypotheses because of their unusual life history, extraordinary abundance, and wide geographical range. Periodical cicadas provide the best examples of synchronous periodicity and predator satiation in the animal kingdom, and are excellent illustrations of habitat partitioning (by the three morphologically distinct species groups), incipient species (the year classes or broods), and cryptic species (a newly discovered 13‐year species, Magicicada neotredecim). They are particularly useful for exploring questions regarding speciation via temporal isolation, or allochronic speciation. Recently, data were presented that provided strong support for an instance of allochronic speciation by life‐cycle switching. This speciation event resulted in the formation of a new 13‐year species from a 17‐year species and led to secondary contact between two formerly separated lineages, one represented by the new 13‐year cicadas (and their 17‐year ancestors), and the other represented by the pre‐existing 13‐year cicadas. Allozyme frequency data, mitochondrial DNA (mtDNA), and abdominal colour were shown to be correlated genetic markers supporting the life‐cycle switching/allochronic speciation hypothesis. In addition, a striking pattern of reproductive character displacement in male call pitch and female pitch preference between the two 13‐year species was discovered. In this paper we report a strong association between calling song pitch and mtDNA haplotype for 101 individuals from a single locality within the M. tredecim/M. neotredecim contact zone and a strong association between abdomen colour and mtDNA haplotype. We conclude by reviewing proposed mechanisms for allochronic speciation and reproductive character displacement.

Evidence for paternal leakage in hybrid periodical cicadas (Hemiptera: Magicicada spp.).

Mitochondrial inheritance is generally assumed to be maternal. However, there is increasing evidence of exceptions to this rule, especially in hybrid crosses. In these cases, mitochondria are also inherited paternally, so “paternal leakage” of mitochondria occurs. It is important to understand these exceptions better, since they potentially complicate or invalidate studies that make use of mitochondrial markers. We surveyed F1 offspring of experimental hybrid crosses of the 17-year periodical cicadas Magicicada septendecim, M. septendecula, and M. cassini for the presence of paternal mitochondrial markers at various times during development (1-day eggs; 3-, 6-, 9-week eggs; 16-month old 1st and 2nd instar nymphs). We found evidence of paternal leakage in both reciprocal hybrid crosses in all of these samples. The relative difficulty of detecting paternal mtDNA in the youngest eggs and ease of detecting leakage in older eggs and in nymphs suggests that paternal mitochondria proliferate as the eggs develop. Our data support recent theoretical predictions that paternal leakage may be more common than previously estimated.

Steady Plio-Pleistocene diversification and a 2-million-year sympatry threshold in a New Zealand cicada radiation.

Estimation of diversification rates in evolutionary radiations requires a complete accounting of cryptic species diversity. The rapidly evolving songs of acoustically signaling insects make them good model organisms for such studies. This paper examines the timing of diversification of a large (30 taxon) group of New Zealand cicadas (genus Kikihia Dugdale). We use Bayesian relaxed-clock methods and phylogenetic trees based on nuclear and mitochondrial DNA data, and we apply alternative combinations of evolutionary rate priors and geological calibrations. The extant Kikihia taxa began to diversify near the Miocene/Pliocene boundary around the time of increased mountain-building, and both the mitochondrial and nuclear-gene trees confirm early splits of lineages currently represented by lowland forest-dwelling taxa. Most lineages originated in the Pleistocene, and sustained diversification occurred rapidly at over 0.5 lineages/my, a rate comparable to that of the Hawaiian silverswords. Diversification rate tests suggest an increase in the early to mid-Pliocene, followed by constant diversification from the Late Pliocene onward. No descendants of the many Pleistocene-age splits have evolved the ability to coexist in sympatry, and, where they do come into contact, hybrid zones have been documented based on acoustic and DNA evidence. In contrast, lineages separated in time by approximately 2Myr often overlap in distribution with no evidence of hybridization. This suggests that at least 2Myr has been required to achieve the level of divergence required for reproductive isolation.

Temporal Separation and Speciation in Periodical Cicadas

Abstract Speciation, the set of processes by which two populations of one species become distinct species, is an important topic in evolutionary biology. It is usually impractical to conduct experiments on how new species form, but occasionally the natural history of a species places it in a context that may be thought of as a “natural experiment” with regard to speciation. One such natural experiment involves the periodical cicadas of eastern North America, a group in which populations have become isolated in time and space. Some of these isolated populations appear to have evolved into distinct genetic lineages. A rare life-cycle switching event brought two such lineages into contact in the relatively recent past, and the two lineages are now behaving as distinct species. This natural experiment provides important insights into species differences and the processes that underlie species formation.

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

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.

Long-range Acoustical Signals, Phonotaxis, and Risk in the Sexual Pair-Forming Behaviors of Okanagana canadensis and O. rimosa (Hemiptera: Cicadidae)

Abstract The sexual behaviors of Okanagana canadensis (Provancher) and O. rimosa (Say) are described. In northern Michigan, O. canadensis is typically found in coniferous vegetation, such as cedars; whereas O. rimosa frequent deciduous vegetation. In both species, males call from stationary perches, and females approach them. Females have no specialized receptivity signals, but both males and females engage in bouts of wing flicking that may be alternative, low-risk signaling. Mating is brief and involves no elaborate courtship. The Okanagana mating system, characterized by male advertisement and female searching, is contrasted with that of Magicicada spp., the periodical cicadas of North America, and discussed in the context of relative risks of signaling and searching behaviors.

Decoding Asymmetries in Reproductive Character Displacement

ABSTRACT Reproductive Character Displacement (RCD) has long been of interest to evolutionary biologists because of its association with speciation and reproductive isolation. Most studies of RCD focus on only a single species; however, when information about the evolutionary responses of two species is available, a possible pattern emerges: RCD often appears to be asymmetrical. Possible causes of displacement asymmetries are varied and include asymmetrical costs of hybridization, constraints, the effects of relative abundance, and extinction. Yet in spite of this variety, further study may show that asymmetries in RCD contain important clues about the interactions pf species in contact zones.

Reconstructing asymmetrical reproductive character displacement in a periodical cicada contact zone.

Selection against costly reproductive interactions can lead to reproductive character displacement (RCD). We use information from patterns of displacement and inferences about predisplacement character states to investigate causes of RCD in periodical cicadas. The 13‐year periodical cicada Magicicada neotredecim exhibits RCD and strong reproductive isolation in sympatry with a closely related 13‐year species, Magicicada tredecim. Displacement is asymmetrical, because no corresponding pattern of character displacement exists within M. tredecim. Results from playback and hybridization experiments strongly suggest that sexual interactions between members of these species were possible at initial contact. Given these patterns, we evaluate potential sources of selection for displacement. One possible source is ‘acoustical interference’, or mate‐location inefficiencies caused by the presence of heterospecifics. Acoustical interference combined with the species‐specificity of song pitch and preference appears to predict the observed asymmetrical pattern of RCD in Magicicada. However, acoustical interference does not appear to be a complete explanation for displacement in Magicicada, because our experiments suggest a significant potential for direct sexual interactions between these species before displacement. Another possible source of selection for displacement is hybrid failure. We evaluate the attractiveness of inferred hybrid mating signals, and we examine the viability of hybrid eggs. Neither of these shows strong evidence of hybrid inferiority. We conclude by presenting a model of hybrid failure related to life cycle differences in Magicicada.

Developmental Plasticity of Life-Cycle Length in Thirteen-Year Periodical Cicadas (Hemiptera: Cicadidae)

ABSTRACT Speciation in periodical cicadas (Magicicada Davis) is closely tied to changes in life-cycle length, which presents a paradox because these organisms depend on emergence synchrony for survival. Recently proposed speciation models invoke developmental plasticity as a possible solution: Environmentally triggered “4-yr accelerations” occur in 17-yr cicadas, suggesting that canalization of induced plasticity could change 17-yr populations into temporally isolated 13-yr populations. However, the reverse shift, 13-yr cicadas emerging in 17 yr, has never been documented. We searched 4 yr after the normal emergence of a 13-yr brood (and in a year with no expected periodical cicada emergences anywhere) and found periodical cicadas active at 26 of 92 sites, with examples of all four 13-yr species. At one location, we found evidence of at least 1,724 cicadas per ha emerging. Few males were heard singing at most sites, so these off-schedule cicadas apparently did not survive long in the face of predation. We also found one 13-yr species singing 8 yr late within the range of a different 13-yr brood, suggesting an 8-yr delayed emergence or consecutive generations of 4-yr delayed cicadas. Developmental plasticity in life-cycle length seems to be similar in 13- and 17-yr cicadas—both types possess the ability to switch to the opposite life cycle and to emerge 1 yr early and/or late. The confirmation of a reverse life-cycle switch in 13- cicadas suggests improvements to theories of life-cycle evolution in Magicicada and strengthens the case for developmental plasticity in speciation.

Inflation of Molecular Clock Rates and Dates: Molecular Phylogenetics, Biogeography, and Diversification of a Global Cicada Radiation from Australasia (Hemiptera: Cicadidae: Cicadettini)

Dated phylogenetic trees are important for studying mechanisms of diversification, and molecular clocks are important tools for studies of organisms lacking good fossil records. However, studies have begun to identify problems in molecular clock dates caused by uncertainty of the modeled molecular substitution process. Here we explore Bayesian relaxed-clock molecular dating while studying the biogeography of ca. 200 species from the global cicada tribe Cicadettini. Because the available fossils are few and uninformative, we calibrate our trees in part with a cytochrome oxidase I (COI) clock prior encompassing a range of literature estimates for arthropods. We show that tribe-level analyses calibrated solely with the COI clock recover extremely old dates that conflict with published estimates for two well-studied New Zealand subclades within Cicadettini. Additional subclade analyses suggest that COI relaxed-clock rates and maximum-likelihood branch lengths become inflated relative to EF-1[Formula: see text] intron and exon rates and branch lengths as clade age increases. We present corrected estimates derived from: (i) an extrapolated EF-1[Formula: see text] exon clock derived from COI-calibrated analysis within the largest New Zealand subclade; (ii) post hoc scaling of the tribe-level chronogram using results from subclade analyses; and (iii) exploitation of a geological calibration point associated with New Caledonia. We caution that considerable uncertainty is generated due to dependence of substitution estimates on both the taxon sample and the choice of model, including gamma category number and the choice of empirical versus estimated base frequencies. Our results suggest that diversification of the tribe Cicadettini commenced in the early- to mid-Cenozoic and continued with the development of open, arid habitats in Australia and worldwide. We find that Cicadettini is a rare example of a global terrestrial animal group with an Australasian origin, with all non-Australasian genera belonging to two distal clades. Within Australia, we show that Cicadettini is more widely distributed than any other cicada tribe, diverse in temperate, arid and monsoonal habitats, and nearly absent from rainforests. We comment on the taxonomic implications of our findings for thirteen cicada genera.