Kathy B. R. Hill

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.

Glacial refugia in a maritime temperate climate: Cicada (Kikihia subalpina) mtDNA phylogeography in New Zealand

Understanding the biological significance of Pleistocene glaciations requires knowledge of the nature and extent of habitat refugia during glacial maxima. An opportunity to examine evidence of glacial forest refugia in a maritime, Southern Hemisphere setting is found in New Zealand, where the extent of Pleistocene forests remains controversial. We used the mitochondrial phylogeography of a forest‐edge cicada (Kikihia subalpina) to test the hypothesis that populations of this species survived throughout South Island during the Last Glacial Maximum. We also compared mitochondrial DNA phylogeographic patterns with male song patterns that suggest allopatric divergence across Cook Strait. Cytochrome oxidase I and II sequences were analyzed using network analysis, maximum‐likelihood phylogenetic estimation, Bayesian dating and Bayesian skyline plots. K. subalpina haplotypes from North Island and South Island form monophyletic clades that are concordant with song patterns. Song divergence corresponds to approximately 2% genetic divergence, and Bayesian dating suggests that the North Island and South Island population‐lineages became isolated around 761 000 years bp. Almost all South Island genetic variation is found in the north of the island, consistent with refugia in Marlborough Sounds, central Nelson and northwest Nelson. All central and southern South Island and Stewart Island haplotypes are extremely similar to northern South Island haplotypes, a ‘northern richness/southern purity’ pattern that mirrors genetic patterns observed in many Northern Hemisphere taxa. Proposed southern South Island forest habitat fragments may have been too small to sustain populations of K. subalpina, and/or they may have harboured ecological communities with no modern‐day analogues.

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.

Systematic revision of the genus Psithyristria Stål (Hemiptera: Cicadidae) with seven new species and a molecular phylogeny of the genus and higher taxa

The cicada genus Psithyristria Stål (Hemiptera: Cicadidae), endemic to Luzon, the Philippines, is reviewed, and its higher taxonomic affiliations are determined using morphology and molecular phylogenetics. Seven new Psithyristria species, P. grandis, sp.n., P. albiterminalis, sp.n., P. incredibilis, sp.n., P. paraspecularis, sp.n., P. peculiaris, sp.n., P. moderabilis, sp.n. and P. genesis, sp.n., are described. A key to the 12 known species is provided. The molecular phylogenetic analyses of Psithyristria and putatively related taxa showed some unexpected generic relationships, leading to changes in higher taxonomic placement for a number of Asian cicada genera. Psithyristria falls within the tribe Cicadini Latreille, 1802, and the tribe Psithyristriini Distant, 1905 syn.n. is therefore synonymized with Cicadini. The subtribe Psithyristriina Distant, 1905 stat.n. is recognized within Cicadini and defined for the genera Psithyristria, transferred from Psithyristriini, and Basa Distant, Pomponia Stål and Semia Matsumura, transferred from Cicadina, synonymizing Pomponiina Kato, 1932syn.n. with Psithyristriina. The Cicadini subtribe Leptopsaltriina Moulton, 1923 is redefined to include the genera Terpnosia Distant, Euterpnosia Matsumura, Leptosemia Matsumura, Neocicada Kato, Puranoides Moulton, Leptopsaltria Stål, Tanna Distant, Purana Distant, Formosemia Matsumura, Maua Distant, Nabalua Moulton, Taiwanosemia Matsumura, Gudaba Distant and Calcagninus Distant, synonymizing Terpnosiina Kato, 1932syn.n. The tribe Cicadatrini Distant, 1905 is recognized and redefined to include the genera Cicadatra Kolenati, Psalmocharias Kirkaldy, Mogannia Amyot & Audinet‐Serville, Nipponosemia Kato and Emathia Stål, synonymizing Moganniini Distant, 1905 syn.n. The nine Psithyristria species included in the molecular analyses have an uncorrected mitochondrial genetic distance of 2–9%, and most species appear to be related through a single radiation event that occurred approximately 5–10 Ma. No phylogenetic structure was found in two unusually divergent characters, the forewing venation and the shape of the uncal lobes. Psithyristria is found in the northern Luzon mountains and is closely related to Semia of Taiwan and eastern China, Pomponia of east Asia and the Indonesian/Malaysian islands, and probably most closely to Basa of India. Psithyristria may be a cicadid example of a small number of Philippine organisms that trace their ancestry directly back to the temperate Asian mainland, rather than through the island chains to the south of the country.

Versatile aggressive mimicry of cicadas by an Australian predatory katydid.

Background In aggressive mimicry, a predator or parasite imitates a signal of another species in order to exploit the recipient of the signal. Some of the most remarkable examples of aggressive mimicry involve exploitation of a complex signal-response system by an unrelated predator species. Methodology/Principal Findings We have found that predatory Chlorobalius leucoviridis katydids (Orthoptera: Tettigoniidae) can attract male cicadas (Hemiptera: Cicadidae) by imitating the species-specific wing-flick replies of sexually receptive female cicadas. This aggressive mimicry is accomplished both acoustically, with tegminal clicks, and visually, with synchronized body jerks. Remarkably, the katydids respond effectively to a variety of complex, species-specific Cicadettini songs, including songs of many cicada species that the predator has never encountered. Conclusions/Significance We propose that the versatility of aggressive mimicry in C. leucoviridis is accomplished by exploiting general design elements common to the songs of many acoustically signaling insects that use duets in pair-formation. Consideration of the mechanism of versatile mimicry in C. leucoviridis may illuminate processes driving the evolution of insect acoustic signals, which play a central role in reproductive isolation of populations and the formation of species.

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.

Limited, episodic diversification and contrasting phylogeography in a New Zealand cicada radiation

BackgroundThe New Zealand (NZ) cicada fauna contains two co-distributed lineages that independently colonized the isolated continental fragment in the Miocene. One extensively studied lineage includes 90% of the extant species (Kikihia + Maoricicada + Rhodopsalta; ca 51 spp.), while the other contains just four extant species (Amphipsalta – 3 spp. + Notopsalta – 1 sp.) and has been little studied. We examined mitochondrial and nuclear-gene phylogenies and phylogeography, Bayesian relaxed-clock divergence timing (incorporating literature-based uncertainty of molecular clock estimates) and ecological niche models of the species from the smaller radiation.ResultsMitochondrial and nuclear-gene trees supported the monophyly of Amphipsalta. Most interspecific diversification within Amphipsalta-Notopsalta occurred from the mid-Miocene to the Pliocene. However, interspecific divergence time estimates had large confidence intervals and were highly dependent on the assumed tree prior, and comparisons of uncorrected and patristic distances suggested difficulty in estimation of branch lengths. In contrast, intraspecific divergence times varied little across analyses, and all appear to have occurred during the Pleistocene. Two large-bodied forest taxa (A. cingulata, A. zelandica) showed minimal phylogeographic structure, with intraspecific diversification dating to ca. 0.16 and 0.37 Ma, respectively. Mid-Pleistocene-age phylogeographic structure was found within two smaller-bodied species (A. strepitans – 1.16 Ma, N. sericea – 1.36 Ma] inhabiting dry open habitats. Branches separating independently evolving species were long compared to intraspecific branches. Ecological niche models hindcast to the Last Glacial Maximum (LGM) matched expectations from the genetic datasets for A. zelandica and A. strepitans, suggesting that the range of A. zelandica was greatly reduced while A. strepitans refugia were more extensive. However, no LGM habitat could be reconstructed for A. cingulata and N. sericea, suggesting survival in microhabitats not detectable with our downscaled climate data.ConclusionsUnlike the large and continuous diversification exhibited by the Kikihia-Maoricicada-Rhodopsalta clade, the contemporaneous Amphipsalta-Notopsalta lineage contains four comparatively old (early branching) species that show only recent diversification. This indicates either a long period of stasis with no speciation, or one or more bouts of extinction that have pruned the radiation. Within Amphipsalta-Notopsalta, greater population structure is found in dry-open-habitat species versus forest specialists. We attribute this difference to the fact that NZ lowland forests were repeatedly reduced in extent during glacial periods, while steep, open habitats likely became more available during late Pleistocene uplift.

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 (Hemiptera: Auchenorrhyncha: Cicadidae)

North America has a diverse cicada fauna with multiple genera from all three Cicadidae subfamilies, yet molecular phylogenetic analyses have been completed only for the well-studied periodical cicadas (Magicicada Davis). The genus Tibicen Latreille, a large group of charismatic species, is in need of such work because morphological patterns suggest multiple groups with complicated relationships to other genera in the tribe Cryptotympanini. In this paper we present a molecular phylogenetic analysis, based on mitochondrial and nuclear DNA, of 35 of the 38 extant USA species and subspecies of the genus Tibicen together with their North American tribal allies (Cornuplura Davis, Cacama Davis), selected Tibicen species from Eurasia, and representatives of other Eurasian and Pacific cryptotympanine genera. This tree shows that Tibicen contains several well-supported clades, one predominating in eastern and central North America and related to Cryptotympana Stål and Raiateana Boulard, another in western North America related to Cacama and Cornuplura, and at least two clades in Eurasia. We also present a morphological cladistic analysis of Tibicen and its close allies based on 27 characters. Character states identified in the cladistic analysis define three new genera, two for North American taxa (Hadoa gen. n. and Neotibicen gen. n.) including several Mexican species, and one for Asian species (Subsolanus gen. n.). Using relaxed molecular clocks and literature-derived mtDNA rate estimates, we estimate the timeframe of diversification of Tibicen clades and find that intergeneric divergence has occurred since the late Eocene, with most extant species within the former Tibicen originating after the mid-Miocene. We review patterns of ecology, behavior, and geography among Tibicen clades in light of the phylogenetic results and note that the study of these insects is still in its early stages. Some Mexican species formerly placed in Tibicen are here transferred to Diceroprocta, following refinement of the definition of that genus.