Evidence for differential assortative female preference in association with refugial isolation of rainbow skinks in Australia's tropical rainforests

Copyright: © 2008 Dolman. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.Divergence driven by female preference can give rise to pre-mating isolation more rapidly than post-mating isolation can evolve through the accumulation of allelic incompatibilities. Moreover pre-mating isolation may be more effective at maintaining morphological differentiation between divergent populations. In the context of Australian rainforest endemic skinks that were historically subjected to refugial isolation, this study examined the following predictions: 1) that assortative female preference is associated with more recent divergence of southern C. rubrigularis (S-RED) and C. rhomboidalis (BLUE), but not with deeply divergent S-RED and northern C. rubrigularis (N-RED); and 2) that upon secondary contact, morphological differentiation is maintained between S-RED and BLUE, whereas N-RED and S-RED remain morphogically indistinguishable. Principal Findings Female preference trials found no evidence for assortative female preference between N-RED and S-RED, supporting a previous genetic hybrid zone study which inferred post-mating but no pre-mating isolation. In contrast there is evidence for assortative female preference between S-RED and BLUE, with BLUE females preferring to associate with BLUE males, but S-RED females showing no preference. Multi-locus coalescent analyses, used to estimate post-divergence gene-flow between proximally located S-RED and BLUE populations, rejected zero gene-flow from BLUE to S-RED and thus RED and BLUE have maintained morphological differentiation despite secondary contact. Morphometric analyses confirmed a lack of morphological divergence between N-RED and S-RED and established that BLUE is morphologically divergent from RED in traits other than throat colour. Conclusions/Significance Long-term isolation has been sufficient to generate post-mating isolation but no morphological divergence between N-RED and S-RED. In contrast, greater morphological differentiation is associated with evidence for assortative female preference between more recently diverged S-RED and BLUE. Combined with previous estimates of lineage-wide gene flow, these results are consistent with the suggestion that assortative female preference is more effective than post-mating isolation in maintaining morphological differentiation between divergent populations.Gaynor Dolma

Morphological differentiation between N-RED, S-RED and BLUE.

<p>Canonical centroid plots from discriminant analyses for a) females; and b) males. All parameter variables: log snout vent length (SVL), head width (HW), hind limb tibia length (TL) are represented as vectors, with the length of each vector indicating its ability to separate the groups and its direction assists in the interpretation of these differences. Circles represent the 95% confidence intervals around the lineage's centroid.</p

Observation enclosure used for female preference trials.

<p>Solid walls extend into the female's quadrant between the two males to form visual barriers so that the female can only see the male in the quadrant she is in (diagonal grey dashed lines mark the line of sight).</p

Phylogenetic relationships and spatial distributions of the three lineages of rainbow skinks.

<p>A) Phylogenetic relationships among N-RED, S-RED and BLUE according to mitochondrial gene (ND4) maximum likelihood tree <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003499#pone.0003499-Dolman1" target="_blank">[20]</a>. B) The map shows the extent of Wet Tropics and Mid-east Queensland rainforest, and the biogeographical distribution of each of the three Carlia lineages. The shades of lineages on the phylogeny correlate with shades of biogeographic distributions in the map of north-eastern Australia: N-RED in black, S-RED in hashed and BLUE in grey. For female preference trials, three populations from each lineage were collected: N-RED from Windsor Uplands (WU), Carbine Uplands (CU) northern Lamb Uplands (LU); S-RED from northern and southern Atherton Uplands (AU), Spec Uplands (SU); and BLUE from Mt. Elliot (EU), and Finch Hatton in the Clarke Ranges and Brandy Creek in the Conway Ranges in mid-east Queensland (MEQ). Refer to supplementary online material for specific location details. For population demographic analyses, individuals of S-RED were from Spec Uplands (SU) and Halifax Uplands (HU), and BLUE were from Mt. Elliot (EU), and Magnetic Island (MI).</p

Photographs of typical males showing throat colour difference between the red and blue throated rainbow skinks.

<p>A) The red throated rainbow skink, <i>Carlia rubrigularis</i> (RED) (N-RED and S-RED are indistinguishable) and B) the blue throated rainbow skink, <i>C. rhomboidalis</i> (BLUE). Throat coloration is present in both males and females in the breeding season, but is more vivid in adult males and often absent in females. Photographs: Anthony O'Toole, University of Queensland.</p

clarum_noST_SB_EBSP

EBSP xml infile for Cinclosoma clarum (putative Cinclosoma clarum fordianum removed) run in Beast v1.7.5. EBSP run uses mtDNA rate and one nuclear loci. This was chosen based on locus closest to average of all loci. All loci (except one) are within the bounds of the Ellegren (2013) Annual Review of Ecology and Systematics. The one outside is only a tiny fraction lower

clarum_noST_SB_EBSP

EBSP xml infile for Cinclosoma clarum (putative Cinclosoma clarum fordianum removed) run in Beast v1.7.5. EBSP run uses mtDNA rate and one nuclear loci. This was chosen based on locus closest to average of all loci. All loci (except one) are within the bounds of the Ellegren (2013) Annual Review of Ecology and Systematics. The one outside is only a tiny fraction lower

castanotum_EBSP

EBSP xml infile for Cinclosoma castanotum run in Beast v1.7.5. EBSP run uses mtDNA rate and one nuclear loci. This was chosen based on locus closest to average of all loci. All loci (except one) are within the bounds of the Ellegren (2013) Annual Review of Ecology and Systematics. The one outside is only a tiny fraction lower

Cinclosoma _Codominant

Geneland Infile: Diploid genotype file for has 22 columns (11 nulear loci), sequencing data converted to allelic data, missing data= NA, comma delimited