Evolutionary dynamics of a cycad obligate pollination mutualism – Pattern and process in extant Macrozamia cycads and their specialist thrips pollinators

[Display omitted] •A dozen Eastern Australian endemic Macrozamia cycads are pollinated only by thrips assigned to the genus Cycadothrips.•The evolutionary history of Cycadothrips was explored using phylogenetic and microsatellite-based gene flow analyses.•Cycadothrips are revealed to be extremely host specific and have diversified recently, at a similar time to their hosts.•Host switching and cospeciation in allopatry, rather than coevolution, appear to be the dominant processes.•Cycadothrips chadwicki may represent as many as five cryptic species. Obligate pollination mutualisms are rare and few have been investigated deeply. This paper focuses on one such mutualism involving thrips in the genus Cycadothrips that pollinate cycads in the genus Macrozamia. Both represent old lineages relative to insects and plants generally, are endemic to Australia, and are mutually co-dependent. The phylogenetic analyses presented here demonstrate that the pollinator is much more diverse than previously considered, with each pollinator lineage being extremely specific to between one and three host species where these latter share part of their distribution. The new species diversity we demonstrate in Cycadothrips all presently falls under the species name C. chadwicki, and these different lineages diversified during two periods. An older divergence, beginning 7.3Mya (4.4–11.1, 95% HPD), resulted in three major lineages, and then further diversification within each of these three lineages took place at most 1.1Mya (0.6–1.8, 95% HPD). These divergence estimates correspond to times when aridification was increasing in Australia, suggesting that population fragmentation following climatic change has played a significant role in the evolutionary history of Cycadothrips and Macrozamia. This means that co-diversification of the host and pollinator in allopatry appears to be the dominant process affecting species diversity. Host switching is also clearly evident in the discrepancy between the divergence times of the C. chadwicki lineage and C. albrechti, about 10.8Mya (6.0–17.1, 95% HPD), and their hosts, at about 1.1Mya (0.2–3.4Mya, 95% HPD), in that the pollinator split pre-dates the origin of the associated host species of each. These results add to the body of evidence that the evolutionary processes important in obligate pollinator mutualisms are more varied than previously assumed.