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Phylogenomics of a rapid radiation: the Australian rainbow skinks.

ABSTRACT: The application of target capture with next-generation sequencing now enables phylogenomic analyses of rapidly radiating clades of species. But such analyses are complicated by extensive incomplete lineage sorting, demanding the use of methods that consider this process explicitly, such as the multispecies coalescent (MSC) model. However, the MSC makes strong assumptions about divergence history and population structure, and when using the full Bayesian implementation, current computational limits mean that relatively few loci and samples can be analysed for even modest sized radiations. We explore these issues through analyses of an extensive (>?1000 loci) dataset for the Australian rainbow skinks. This group consists of 3 genera and 41 described species, which likely diversified rapidly in Australia during the mid-late Miocene to occupy rainforest, woodland, and rocky habitats with corresponding diversity of morphology and breeding colouration. Previous phylogenetic analyses of this group have revealed short inter-nodes and high discordance among loci, limiting the resolution of inferred trees. A further complication is that many species have deep phylogeographic structure - this poses the question of how to sample individuals within species for analyses using the MSC.Phylogenies obtained using concatenation and summary coalescent species tree approaches to the full dataset are well resolved with generally consistent topology, including for previously intractable relationships near the base of the clade. As expected, branch lengths at the tips are substantially overestimated using concatenation. Comparisons of different strategies for sampling haplotypes for full Bayesian MSC analyses (for one clade and using smaller sets of loci) revealed, unexpectedly, that combining haplotypes across divergent phylogeographic lineages yielded consistent species trees.This study of more than 1000 loci provides a strongly-supported estimate of the phylogeny of the Australian rainbow skinks, which will inform future research on the evolution and taxonomy of this group. Our analyses suggest that species tree estimation with the MSC can be quite robust to violation of the assumption that the individuals representing a taxon are sampled from a panmictic population.

SUBMITTER: Bragg JG

PROVIDER: S-EPMC5800007 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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Phylogenomics of a rapid radiation: the Australian rainbow skinks.

Bragg Jason G JG Potter Sally S Afonso Silva Ana C AC Hoskin Conrad J CJ Bai Benjamin Y H BYH Moritz Craig C

BMC evolutionary biology 20180205 1

<h4>Background</h4>The application of target capture with next-generation sequencing now enables phylogenomic analyses of rapidly radiating clades of species. But such analyses are complicated by extensive incomplete lineage sorting, demanding the use of methods that consider this process explicitly, such as the multispecies coalescent (MSC) model. However, the MSC makes strong assumptions about divergence history and population structure, and when using the full Bayesian implementation, current ...[more]

PMID: 29402211

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Project description:While methods for genetic species delimitation have noticeably improved in the last decade, this remains a work in progress. Ideally, model based approaches should be applied and considered jointly with other lines of evidence, primarily morphology and geography, in an integrative taxonomy framework. Deep phylogeographic divergences have been reported for several species of Carlia skinks, but only for some eastern taxa have species boundaries been formally tested. The present study does this and revises the taxonomy for two species from northern Australia, Carlia johnstonei and C. triacantha. We introduce an approach that is based on the recently published method StarBEAST2, which uses multilocus data to explore the support for alternative species delimitation hypotheses using Bayes Factors (BFD). We apply this method, jointly with two other multispecies coalescent methods, using an extensive (from 2,163 exons) data set along with measures of 11 morphological characters. We use this integrated approach to evaluate two new candidate species previously revealed in phylogeographic analyses of rainbow skinks (genus Carlia) in Western Australia. The results based on BFD StarBEAST2, BFD* SNAPP and BPP genetic delimitation, together with morphology, support each of the four recently identified Carlia lineages as separate species. The BFD StarBEAST2 approach yielded results highly congruent with those from BFD* SNAPP and BPP. This supports use of the robust multilocus multispecies coalescent StarBEAST2 method for species delimitation, which does not require a priori resolved species or gene trees. Compared to the situation in C. triacantha, morphological divergence was greater between the two lineages within Kimberley endemic C. johnstonei, which also had deeper divergent histories. This congruence supports recognition of two species within C. johnstonei. Nevertheless, the combined evidence also supports recognition of two taxa within the more widespread C. triacantha. With this work, we describe two new species, Carlia insularis sp. nov and Carlia isostriacantha sp. nov. in the northwest of Australia. This contributes to increasing recognition that this region of tropical Australia has a rich and unique fauna.

Project description:BackgroundDivergence 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 findingsFemale 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/significanceLong-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.

Project description:Background and aimsThe centropogonid clade (Lobelioideae: Campanulaceae) is an Andean-centred rapid radiation characterized by repeated convergent evolution of morphological traits, including fruit type and pollination syndromes. While previous studies have resolved relationships of lineages with fleshy fruits into subclades, relationships among capsular species remain unresolved. This lack of resolution has impeded reclassification of non-monophyletic genera, whose current taxonomy relies heavily on traits that have undergone convergent evolution.MethodsTargeted sequence capture using a probe-set recently developed for the centropogonid clade was used to obtain phylogenomic data from DNA extracted from both silica-dried and herbarium leaf tissue. These data were used to infer relationships among species using concatenated and partitioned species tree methods, and to quantify gene tree discordance.Key resultsWhile silica-dried leaf tissue resulted in longer assembled sequence data, the inclusion of herbarium samples improved taxonomic representation. Relationships among baccate lineages are similar to those inferred in previous studies, although they differ for lineages within and among capsular clades. We improve the phylogenetic resolution of Siphocampylus, which forms ten groups of closely related species which we informally name. Two subclades of Siphocampylus and two individual species are rogue taxa whose placement differs widely across analyses. Gene tree discordance (including cytonuclear discordance) is rampant.ConclusionsThis first phylogenomic study of the centropogonid clade considerably improves our understanding of relationships in this rapid radiation. Differences across analyses and the possibility of additional lineage discoveries still hamper a solid and stable reclassification. Rapid morphological innovation corresponds with a high degree of phylogenomic complexity, including cytonuclear discordance, nuclear gene tree conflict and well-supported differences between analyses based on different nuclear loci. Together, these results point to a potential role of hemiplasy underlying repeated convergent evolution. This hallmark of rapid radiations is probably present in many other species-rich Andean plant radiations.

Dataset Information

Phylogenomics of a rapid radiation: the Australian rainbow skinks.

Publications

Phylogenomics of a rapid radiation: the Australian rainbow skinks.

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