‘Mainland-island’ population structure of a terrestrial salamander in a forest-bocage landscape with little evidence for in situ ecological speciation

Abstract

Adaptation to different ecological environments can, through divergent selection, generate phenotypic and genetic differences between populations, and eventually give rise to new species. The fire salamander (Salamandra salamandra) has been proposed to represent an early stage of ecological speciation, driven by differential habitat adaptation through the deposition and development of larvae in streams versus ponds in the Kottenforst near Bonn (Germany). We set out to test this hypothesis of ecological speciation in an area different from the one where it was raised and we took the opportunity to explore for drivers of genetic differentiation at a landscape scale. A survey over 640 localities demonstrated the species' presence in ponds and streams across forests, hilly terrain and areas with hedgerows ('bocage'). Genetic variation at 14 microsatellite loci across 41 localities in and around two small deciduous forests showed that salamander effective population sizes were higher in forests than in the bocage, with panmixia in the forests (F st < 0.010) versus genetic drift or founder effects in several of the small and more or less isolated bocage populations (F st > 0.025). The system fits the 'mainlandisland' metapopulation model rather than indicating adaptive genetic divergence in pond versus stream larval habitats. A reanalysis of the Kottenforst data indicated that microsatellite genetic variation fitted a geographical rather than an environmental axis, with a sharp transition from a western pondbreeding to an eastern, more frequently stream-breeding group of populations. A parallel changeover in mitochondrial DnA exists but remains to be well documented. the data support the existence of a hybrid zone following secondary contact of differentiated lineages, more so than speciation in situ. Adaptation to different ecological environments can, through divergent selection, generate phenotypic and genetic differences between populations. These changes may eventually give rise to new species. The speciation process is often quantitative in nature, as illustrated by numerous studies showing that divergence during speciation varies continuously, and the sequence of genetically-based changes that occur as two lineages on the pathway to reproductive isolation diverge from one another has been coined the 'speciation continuum' 1,2. Divergent evolution and reproductive isolation are the primary elements of the speciation continuum, but many have recognized that reproductive isolation is usually a signature effect rather than a primary cause of speciation. Whereas the mechanisms underlying reproductive isolation are by now mostly well understood (such as natural and sexual selection and genetic drift due to founder events, etc.), biologists continue to struggle with understanding how and why these evolutionary processes cause the disjoined genetic connections that are integral to the emergence of new species, in particular in conditions of sympatry 3-6. Organisms that are organized in deme-structured metapopulations, w...

Physical and ecological isolation contribute to maintain genetic differentiation between fire salamander subspecies

“…Landcover-based models, on the other hand, always behaved similarly between regions, improving, although slightly, genetic differentiation predictions from IBD models in the ICS and MTR (Table S5). If we consider this together with the fact that forest cover had the highest weight in landcover ENMs (Table S6), our results add to the cumulative evidence that forested areas play a key role in genetic connectivity in salamander populations (Cushman 2006;Antunes et al 2018;Emel et al 2019;Lourenço et al 2019;Arntzen and van Belkom 2020).…”

“…Nonetheless, subspecies differentiation seems to be maintained in the Eastern ICS by the combined effect of physical and ecological isolation. Examples from S. salamandra ecotypes in which gene flow is restricted by processes of ecological divergence have already been documented in parapatric pond-and stream-breeding fire salamanders across the Kottenforst (Hendrix et al 2017; but see Arntzen and van Belkom 2020).…”

Demography and spatial activity of fire salamanders, Salamandra salamandra (Linnaeus, 1758), in two contrasting habitats in the Vienna Woods

“…Breeding in stagnant water bodies may be more common in fire salamanders than generally recognized, also in the western subspecies S. s. terrestris (Denoël and Winandy 2014;Arntzen and van Belkom 2020). A comparison of the well-studied situation in the Kottenforst with that in Vienna does not support generalisations about stream-breeding versus pond-breeding populations but suggests that local environmental conditions shape the variation in life history traits.…”

“…In this population, genetically divergent subpopulations associated with larval habitat types -ponds versus streams -differ in several life-history traits (Caspers et al 2014;Oswald et al 2020), including movement behaviour (Hendrix et al 2017). The interpretation of this situation as an example of in situ adaptive divergence, possibly a first step in ecological speciation (Steinfartz et al 2007), was recently challenged by Arntzen and van Belkom (2020), who suggested that the genetic data point to a secondary contact of differentiated lineages.…”

Sex chromosomes as supergenes of speciation: why amphibians defy the rules?

“…The high speciation rates in this group nevertheless still associates with their diversity in coloration and the role it plays in aposematic mimicry [122,123]. In fire salamanders, the genetic structure between populations inhabiting distinct habitats was hypothesized to reflect nascent ecological speciation [124], although the pattern can be explained by isolation-by-distance [125]. In European amphibians, hybrid zone analyses suggest that speciation proceeds from genomic divergence in allopatry, generating post-zygotic barriers between cryptic species long before the divergence of sexual traits responsible for pre-mating isolation in sympatry [126,127] (see also §4(c)).…”