How the Aridification of Australia Structured the Biogeography and Influenced the Diversification of a Large Lineage of Australian Cicadas

Abstract

Over the last 30 million years, Australia's landscape has undergone dramatic cooling and drying due to the establishment of the Antarctic Circumpolar Current and change in global CO$_{2}$ levels. Studies have shown that many Australian organisms went extinct during these major cooling events, while others experienced adaptive radiations and increases in diversification rates as a result of exploiting new niches in the arid zone. Despite the many studies on diversification and biogeography in Australia, few have been continent-wide and none have focused on a group of organisms adapted to feeding on plants. We studied 162 species of cicadas in the Australian Pauropsalta complex, a large generic lineage within the tribe Cicadettini. We asked whether there were changes in the diversification rate of Pauropsalta over time and if so: 1) which clades were associated with the rate change? 2) did timing of rate shifts correspond to known periods of dramatic historical climate change, 3) did increases in diversification rate along select lineages correspond to adaptive radiations with movement into the arid zone? To address these questions, we estimated a molecular phylogeny of the Pauropsalta complex using ${\sim}$5300 bp of nucleotide sequence data distributed among five loci (one mtDNA locus and four nDNA loci). We found that this large group of cicadas did not diversify at a constant rate as they spread through Australia; instead the signature of decreasing diversification rate changed roughly around the time of the expansion of the east Antarctic ice sheets ${\sim}$16 Ma and the glaciation of the northern hemisphere ${\sim}$3 Ma. Unlike other Australian taxa, the Pauropsalta complex did not explosively radiate in response to an early invasion of the arid zone. Instead multiple groups invaded the arid zone and experienced rates of diversification similar to mesic-distributed taxa. We found evidence for relictual groups, located in pre-Mesozoic habitat, that have not diversified and continue to reside on mesic hosts in isolated "habitat islands". Future work should focus on groups of similar ages with similar distribution patterns to determine whether this tempo and pattern of diversification and biogeography is consistent with evidence from other phytophagous insects.

Morphological variation, genetic differentiation and phylogeography of the East Asia cicada Hyalessa maculaticollis (Hemiptera: Cicadidae)

“…Because no fossil or geological evidence was available for calibration in Cicadidae, we used the widely accepted molecular clock of the mtDNA gene. Although the use of a molecular clock as the only way for calibrating phylogenetic trees is controversial, it does provide a method for estimating approximate divergence times when no other calibration information is available (Maekawa et al ., ; Hill et al ., ; Marshall et al ., , ; Owen et al ., ). Thus, in this study the proposed conventional mutation rates for the insect mitochondrial COI gene of 2.3% per million years (i.e.…”

“…Their large body size and low dispersal ability make cicadas an excellent group to study phylogeographical patterns and to assess the impact of historical events on the current lineage relationships among different populations (Buckley et al ., ; Arensburger et al ., ; Marshall et al ., , ; Hill et al ., ; Owen et al ., ). The cicada Hyalessa maculaticollis (Motschulsky) has a very wide distribution, ranging from China to Far East Russia, the Korean Peninsula and into Japan (Chou et al ., ; Hayashi & Saisho, ; Wang et al, ).…”

Increased diversification rates are coupled with higher rates of climate space exploration in Australian Acacia (Caesalpinioideae)

“…Macroevolutionary patterns have been linked to historical trends in global and regional climate in many Australian lineages, including elevated speciation in arid‐zone pygopodoid geckos (Brennan & Oliver, ), macropods (Couzens & Prideaux, ), cockroaches (Beasley‐Hall et al , ), and cicadas (Owen et al , ). In plants, the eucalypts provide evidence that climate and historical events are important in explaining species distribution and turnover at the continental scale (Ladiges et al , ; Bui et al , ), and Hakea has expanded coincident with a transition to more open, drought and fire‐prone habitats promoted by aridification (Lamont et al , ; Cardillo et al , ).…”

Tracking niche change through time: simultaneous inference of ecological niche evolution and estimation of contemporary niches

“…We used the climatic history of Australia to generate a priori hypotheses which we then tested against the data. Miller et al (2013) estimated the age of the common ancestor of extant Acacia as 23Ma at the earliest, and since then there have been two key periods of declining temperatures and increasing aridity: a long period from 14-5Ma, followed by a brief warmer and wetter period at the start of the Pliocene, then a second period of aridification through the late Pliocene and through the Pleistocene (Owen et al 2017). So we would expect our method to infer more environmental change for the in situ adaptation events, along the axis of drought tolerance, between 14-5 Ma and shortly after 5 Ma, compared to other periods.…”

“…This allows us to test our inferred patterns of niche evolution against independent data on changing climate. Specifically, there have been three significant drying periods in Australia during the Cenozoic Era: around 28-23 Million years ago (Ma), 14-5 Ma, and shortly after 5 Ma (Owen et al 2017). Our method uses only contemporary species distribution data, plus a phylogeny, so comparison of our results to this climate change history provides an independent test of the usefulness of our method.…”