Hybridization, Mitochondrial DNA Phylogeography, and Prediction of the Early Stages of Reproductive Isolation: Lessons from New Zealand Cicadas (Genus Kikihia)

Abstract

One of the major tenets of the modern synthesis is that genetic differentiation among subpopulations is translated over time into genetic differentiation among species. Phylogeographic exploration is therefore essential to the study of speciation because it can reveal the presence of subpopulations that may go on to become species or that may already represent cryptic species. Acoustic species-specific mating signals provide a significant advantage for the recognition of cryptic or incipient species. Because the majority of species do not have such easily recognized premating signals, data from acoustically signaling species can serve as a valuable heuristic tool. Acoustic signals are also convenient tools for recognizing hybridization events. Here, we demonstrate that evidence of hybridization in the form of intermediate song phenotypes is present in many contact zones between species of the New Zealand grass cicadas of the Kikihia muta species complex and that recurring mitochondrial DNA (mtDNA) introgression has created misleading patterns that make it difficult to identify certain taxa using song or mtDNA alone. In one case, introgression appears to have occurred between allopatric taxa by dispersal of introgressed populations of an intermediary species ("hybridization by proxy"). We also present a comparison of mtDNA-tree- and song-based taxonomies obtained for the K. muta complex. We find that 12 mtDNA candidate species are identified using shifts in phylogenetic branching rate found by a single-threshold mixed Yule-coalescent lineage model, while only 7 candidate species are identified using songs. Results from the Yule-coalescent model are dependent on factors such as the number of modeled thresholds and the inclusion of duplicate haplotypes. Genetic distances within song species reach a maximum at about 0.028 substitutions/site when likely cases of hybridization and introgression are excluded. Large genetic breaks or "gaps" are not observed between some northern (warmer climate) song clades, possibly because climate-induced bottlenecks have been less severe. These results support ongoing calls for multimarker genetic studies as well as "integrative taxonomy" that combines information from multiple character sources, including behavior, ecology, geography, and morphology.

Single-locus species delimitation: a test of the mixed Yule–coalescent model, with an empirical application to Philippine round-leaf bats

“…Thus, interpreting the results from a GMYC analysis requires additional sources of information, such as estimates of N e and SR, sequences of independent loci, and corroboration from morphology. As Marshall et al [13] and others have stated, delimiting species is difficult and unlikely ever to be completely automated, or entirely free of arbitrary decisions. Ultimately, large datasets that integrate multiple character types will be most powerful [15].…”

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<br />(Hemiptera: Auchenorrhyncha: Cicadidae)

“…Few detailed analyses have been made of cryptotympanine songs (for a rare example see Ohya 2004), which often contain complex frequency-modulation and lack the discrete elements that have facilitated interspecific comparisons in other groups (e.g., Marshall et al 2011;Popple 2013). Measurement of frequency-based characters requires samples of high-quality recordings in numbers sufficient for careful study (e.g., Sueur & Aubin 2003).…”

“…These species groups tend to have model-corrected mtDNA (COI) divergences below approximately 0.03 substitutions/site/my (Fig. 3), which was identified as an approximate threshold for songdistinctiveness in New Zealand Kikihia Dugdale (Marshall et al 2011). However, some of the western species (e.g., Hadoa townsendii, H. bifida, and H. simplex) have songs that are similar despite much larger mtDNA distances.…”

A new Neotibicen cicada subspecies (Hemiptera: Cicadidae) from the southeastern USA forms hybrid zones with a widespread relative despite a divergent male calling song

“…Interbreeding between the song-distinctive Neotibicen similaris subspecies helps to demonstrate that even large differences in mate-attracting signals do not necessarily imply a difference in receiver response (Marshall et al 2011;Mendelson & Shaw 2012;Schul 1998), as would be the case if Neotibicen cicadas possessed the speciation-facilitating linkages between male song and female preference genes that have been demonstrated for one cricket genus (Wiley et al 2012). Mate discrimination in Neotibicen based on limited phenotypic divergence likely requires time for selection to operate, and the contexts that lead to this evolution are not yet generally known.…”