Loss of a morph is associated with asymmetric character release in a radiation of woodland salamanders

Background

Distinctly different morphs within the same population of a species are named polymorphisms. They occur frequently in zoology. In addition to sexual dimorphism, different morphs can occur in both sexes of a species. Polymorphism differs from genetic variability in that the individual morphs diverge from each other both phenotypically and genotypically, i.e. no gradual intermediate forms occur. An important hypothesis (S. M. Gray, J. S. McKinnon, 2007) is that polymorphic morphs can form dissimilar niches within a species.

Based on phylogenetic studies using various animal taxa polymorphic species are commonly assumed to undergo faster speciation processes than species without polymorphisms. However phylogenetic trees are often not comprehensive enough, because evolutionary contexts can only be reconstructed in detail using a well resolved phylogeny of a suitable taxon. The authors of the preprint discussed here have therefore examined species of the genus Plethodon (Plethodontidae, Urodela, Amphibia), known as woodland salamanders, being endemic to North America. A biological peculiarity of this group is that it lacks an aquatic larval stage. The species are also known for their tendency to polymorphisms in terms of coloring. There are those with a light stripe along the back and those without a light stripe (Figs1, 2).

 

In woodland salamanders the preprint authors introduced the terms “striped” and “unstriped” (entirely black) to describe the two polymorphic forms (Figs. 1, 2). They additionally used the terms „striped species“ and „unstriped species“ to code the major characters of monomorphic taxa. Several scientific and phylogenetic studies have reconstructed that a majority of monomorphic clades in woodland salamanders can be traced back to polymorphic ancestors and that some unstriped monomorphic taxa still temporarily form a stripe during their early development.

Unstriped monomorphic species have a longer body shape with more trunk vertebrae and a more fossorial lifestyle. It was therefore necessary, as part of this study, to use a better resolved phylogenomic tree to reconstruct evolutionary lines of development, which included more than just one sample per species and datasets with more loci in the tree and the involvement of all extant species, especially for polymorphic species such as Plethodon cinereus (Figs. 1,2).

The authors intended to find out, whether faster phenotypic evolution and speciation rates are triggered by the loss of a polymorphism or whether polymorphic species are characterized by faster speciation rates while monomorphic species show faster phenotypic modifications, as it was assumed by former researchers.

Key findings

The authors constructed a phylogenetic tree with 282 anchored hybrid enrichment loci for 57 species of Plethodon (these are all known extant species) which also included multiple units of some species. Species were assigned to the categories ‘striped’, ‘unstriped’, ‘polymorphic’ and ’other’. According to their reconstruction, eastern Plethodon species probably had a polymorphic ancestor, while the ancestors of all Plethodon and western Plethodon could not be assigned to any of the categories with certainty (Fig. 3). Evolutionary transitions were reconstructed from striped toward polymorphic and from there to unstriped

Phenotypic evolution: Unstriped species evolved faster than polymorphic ones, while striped species had a slower evolution compared to polymorphic ones. According to morphometric traits, unstriped species had more and striped species less elongated body morphologies than polymorphic species.

Lineage diversification is about speciation rates: Based on the author’s reconstructions, unstriped species showed faster diversification rates than polymorphic species and also higher tip speciation rates than striped species. The authors concluded from their findings that polymorphism is not characterized by faster speciation rates, at least not in the taxon Plethodon.

 

What I like about this preprint

The authors were able to use a diverse, but also a kind of compact and thus suitable model to address a topic that researchers in zoology are often confronted with: polymorphisms. The endemic, species-rich salamander genus Plethodon not only enabled the reconstruction of a differentiated phylogenomic tree, but could also be divided into the relatively simple forms ‘striped’ and ‘unstriped’ due to a conserved color polymorphism. This formed an excellent basis to study and discuss evolutionary mechanisms, which are of general interest when thinking about evolutionary mechanisms in all animal taxa.

Questions to the authors

• Unstriped species not only show faster rates of phenotypic evolution, but also tend to have longer body morphologies than polymorphic and striped species. The authors relate this to a more fossorial lifestyle in unstriped species. To what extent can even the unstriped morphs in polymorphic species be assigned to an already stronger fossorial niche formation, and how sympatric or isolated do the morphs of a polymorphic species appear in a population? Are there direct or genomic findings on the frequency of genetic exchange between the different morphs?
• In Plethodon cinereus, in addition to the two morphs striped (redback phase) and unstriped (leadback phase), other color variations also occur, for example albinotic, melanotic or leucistic forms. Do such variants also occur regularly in other polymorphic species, and if so, are such forms evenly distributed among striped and unstriped morphs? One might presume that albino forms could be disadvantaged under certain ecological conditions and therefore appear more frequently in morphs that for example are less fossorial.

Future directions

It is fundamentally a goal of evolutionary studies based on a specific model (Plethodon) to derive evolutionary mechanisms from the results that apply to the entire animal kingdom. Future studies might determine which factors exactly favor the formation and maintenance of a polymorphism in Plethodon species; and which factors favor the elimination of a morph. And after the elimination of a morph, it would be interesting to study which additional features, such as detailed ecological conditions, can influence the increased evolutionary rates. Biological peculiarities of the stem species of Plethodon, for example, might be relevant in this context, such as the lack of an aquatic larval development.

Reference

Gray SM, McKinnon JS. Linking color polymorphism maintenance and speciation. Trends EcolEvol. 2007 Feb;22(2):71-9. Epub 2006 Oct 19. PMID: 17055107. DOI: https://doi.org/10.1016/j.tree.2006.10.005

Tags: evolution, monomorphic, phenotypic evolution, phylogenetic tree, plethodon, polymorphic, polymorphism, speciation, striped, unstriped, woodland salamanders, zoology

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