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, 3 (4), 1031-49

Australasian Sky Islands Act as a Diversity Pump Facilitating Peripheral Speciation and Complex Reversal From Narrow Endemic to Widespread Ecological Supertramp

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Australasian Sky Islands Act as a Diversity Pump Facilitating Peripheral Speciation and Complex Reversal From Narrow Endemic to Widespread Ecological Supertramp

Emmanuel F A Toussaint et al. Ecol Evol.

Abstract

The Australasian archipelago is biologically extremely diverse as a result of a highly puzzling geological and biological evolution. Unveiling the underlying mechanisms has never been more attainable as molecular phylogenetic and geological methods improve, and has become a research priority considering increasing human-mediated loss of biodiversity. However, studies of finer scaled evolutionary patterns remain rare particularly for megadiverse Melanesian biota. While oceanic islands have received some attention in the region, likewise insular mountain blocks that serve as species pumps remain understudied, even though Australasia, for example, features some of the most spectacular tropical alpine habitats in the World. Here, we sequenced almost 2 kb of mitochondrial DNA from the widespread diving beetle Rhantus suturalis from across Australasia and the Indomalayan Archipelago, including remote New Guinean highlands. Based on expert taxonomy with a multigene phylogenetic backbone study, and combining molecular phylogenetics, phylogeography, divergence time estimation, and historical demography, we recover comparably low geographic signal, but complex phylogenetic relationships and population structure within R. suturalis. Four narrowly endemic New Guinea highland species are subordinated and two populations (New Guinea, New Zealand) seem to constitute cases of ongoing speciation. We reveal repeated colonization of remote mountain chains where haplotypes out of a core clade of very widespread haplotypes syntopically might occur with well-isolated ones. These results are corroborated by a Pleistocene origin approximately 2.4 Ma ago, followed by a sudden demographic expansion 600,000 years ago that may have been initiated through climatic adaptations. This study is a snapshot of the early stages of lineage diversification by peripatric speciation in Australasia, and supports New Guinea sky islands as cradles of evolution, in line with geological evidence suggesting very recent origin of high altitudes in the region.

Keywords: Australian region; New Guinea; New Zealand; diversity pump; highlands; peripheral speciation.

Figures

Figure 1
Figure 1
Habitus of Rhantus suturalis (Photo credit: Jan Hamrský)
Figure 2
Figure 2
Habitats and habitus of the Rhantus suturalis southern clade in Southeast Asia and Australasia. Top left: montane peatland pond in Sealy Tarns (∼1300 m) (New Zealand); top right: Welcome River in the North-West of Tasmania; center left: flooded paperbark swamp in Beeliar wetlands (Western Australia); centre right: temporary pool in the Mallee near Balladonia (Western Australia); bottom left: edge of a lake in Ranu Pani (East Java); bottom right: Lake Paniai (1700–3000 m) sheltering R. ekari in West Papua.
Figure 3
Figure 3
Distribution of Rhantus suturalis. Sequence data were not available for the area in red.
Figure 4
Figure 4
Phylogenetic relationships of the Rhantus suturalis species complex Combined dataset with the best-fitting strategy of partitioning under Bayesian Inference. Supports for each node are indicated according to the caption inserted in the figure (BI, Bayesian inference; NJ, neighbor-joining; MP, maximum parsimony; ML, maximum likelihood). A map highlighting collection localities is shown, in which the colors of the spots refer to the respective colored squares underneath the habitus of the different species (e.g., R. riedeli in purple). The major clades are labeled C1 to C7. Names of the species for which a habitus is displayed are specified under the pictures.
Figure 5
Figure 5
Distribution of New Guinean endemic species of the Rhantus suturalis complex. The different colors refer to the distribution of each species except R. suturalis for which they refer to the sampling localities (the distribution of R. suturalis in New Guinea is given by the green areas). The correspondences of the colors are shown in the legend at the bottom left corner of the figure. The asterisk indicates that R. kakapupu was not included in this study.
Figure 6
Figure 6
Network based on the Combined dataset. The locality and the number of specimen(s) are indicated according to the caption. The black dots indicate missing haplotypes.
Figure 7
Figure 7
Simplified network based on the Combined dataset highlighting the New Guinean specimens. The locality and the number of specimen(s) are indicated according to the caption. The black dots indicate missing haplotypes.
Figure 8
Figure 8
Extended Bayesian Skyline Plot based on the rate calculated by Balke et al. (2009). A 500-kyr timescale is shown at the bottom of the chronogram and spans a period of time from the late Pliocene to the present. Result of the Bayesian Skyline Plot is given in the right part of the figure. Demographic expansion and 95%HPD are shown according to the caption.
Figure 9
Figure 9
Maximum credibility tree with mean ages (Ma) from the BEAST analysis. A 1-Ma timescale is shown at the bottom of the chronogram and spans a period of time from the late Miocene to the present. The 95%HPD intervals of divergence times are shown between square brackets for the three major nodes of the chronogram. The vertical bands and pastilles at the nodes of different colors referring to the color of the clades highlight groups of interest for which the names are provided in the top left of the figure. A map with bathymetric information (light blue indicates shallow sea/dark blue indicates deep sea) is shown along with a graphic presenting the evolution of sea level and temperature during the last 7 Ma.

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