Fine-scale genetic structure in a salamander with two reproductive modes: Does reproductive mode affect dispersal?

Lourenço, André; Antunes, Bernardo; Wang, Ian; Velo‐Antón, Guillermo

doi:10.1007/s10682-018-9957-0

Cited by 18 publications

(18 citation statements)

References 72 publications

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“…Substantial genetic drift has been reported for small and isolated populations across its range 31,[53][54][55][56] . We analyzed www.nature.com/scientificreports www.nature.com/scientificreports/ microsatellite genetic data in two metapopulations of the fire salamander in the northwest of Europe, with contrasting results.…”

Section: Discussionmentioning

confidence: 99%

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

Arntzen

Belkom

2020

Sci Rep

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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...

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Section: Discussionmentioning

confidence: 99%

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

Arntzen

Belkom

2020

Sci Rep

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“…It is possible that tadpoles disperse downstream (Eterovick, Yazbeck, Dergam, & Kalapothakis, 2009; Lawson, 2013), but streams inhabited by B. ibitiguara are typically narrow, shallow and frequently partially obstructed (e.g., by fallen trees), which could hamper tadpole dispersal far enough to promote genetic differentiation among patches at a landscape scale. Although detailed quantification of amphibian larval dispersal is sorely needed (Lourenço, Antunes, Wang, & Velo‐Antón, 2018; Wahbe & Bunnell, 2001), evidence suggests that migration/dispersal events of amphibians are primarily made by adults and/or juveniles instead of larvae (Cushman, 2006; Semlitsch, 2008). A similar pattern is also observed in stream fishes, which tend to show restricted movement during most of their lives, causing increased genetic differentiation (Comte & Olden, 2018; Rodríguez, 2002).…”

Section: Discussionmentioning

confidence: 99%

Topography, more than land cover, explains genetic diversity in a Neotropical savanna tree frog

Nali

Becker

Zamudio

et al. 2020

Diversity and Distributions

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Aim Effective conservation policies rely on information about population genetic structure and the connectivity of remnants of suitable habitats. The interaction between natural and anthropogenic discontinuities across landscapes can uncover the relative contributions of different barriers to gene flow, with direct consequences for decision‐making in conservation. We aimed to quantify the relative roles of land cover and topographic variables on the population genetic differentiation and diversity of a stream‐breeding savanna tree frog (Bokermannohyla ibitiguara) across its range. Location Serra da Canastra mountain range, Cerrado of Minas Gerais State, Brazil. Methods We collected samples and extracted DNA samples from 12 populations within and outside a strictly protected park, and used 17 microsatellite markers to assess genetic structure, among‐population differentiation and within‐population diversity measures. We incorporated landscape data derived from digital models and satellite images to create connectivity matrices to correlate with genetic differentiation using Mantel tests. We used generalized linear models and path analyses to assess the roles of each landscape variable in shaping genetic diversity in this species. Results Populations within and outside the park boundaries belonged to four genetic clusters. Most populations showed evidence of limited gene flow, with significant genetic differentiation, except for those within the park, which also had higher levels of allelic richness and heterozygosity. However, genetic differentiation among populations in this landscape was primarily explained by topographic complexity. Likewise, within‐population measures of genetic diversity were best explained by models including elevation and topographic complexity, and not the amount of natural habitat or gallery forests. Main conclusions Our results underscore that topography may be a strong historical factor shaping genetic structure among amphibian populations. Therefore, effective conservation strategies for endangered amphibians should avoid focusing exclusively on habitat suitability, and incorporate topographic complexity, which seems to be a key factor for the fauna of the extremely threatened Brazilian savanna.

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“…The aligned cyt b sequences were trimmed to avoid missing data, resulting in a consensus sequence of 665 bp. Following the protocol used by Lourenço, Antunes, et al (2018), we also amplified 14 microsatel- We tested for deviations from Hardy-Weinberg equilibrium (HWE) and linkage equilibrium (LE) in these microsatellites by performing exact tests in genepop v4.2 (Rousset, 2008; dememorization = 5,000, batch length = 10,000, batch number = 1,000). The p-values from HWE and LE multiple exact tests were corrected using the false discovery rate (Benjamini & Hochberg, 1995).…”

Section: Molecular Markers and Laboratory Proceduresmentioning

confidence: 99%

Comparative landscape genetics reveals the evolution of viviparity reduces genetic connectivity in fire salamanders

et al. 2019

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Evolutionary changes in reproductive mode may affect co‐evolving traits, such as dispersal, although this subject remains largely underexplored. The shift from aquatic oviparous or larviparous reproduction to terrestrial viviparous reproduction in some amphibians entails skipping the aquatic larval stage and, thus, greater independence from water. Accordingly, amphibians exhibiting terrestrial viviparous reproduction may potentially disperse across a wider variety of suboptimal habitats and increase population connectivity in fragmented landscapes compared to aquatic‐breeding species. We investigated this hypothesis in the fire salamander (Salamandra salamandra), which exhibits both aquatic‐ (larviparity) and terrestrial‐breeding (viviparity) strategies. We genotyped 426 larviparous and 360 viviparous adult salamanders for 13 microsatellite loci and sequenced a mitochondrial marker for 133 larviparous and 119 viviparous individuals to compare population connectivity and landscape resistance to gene flow within a landscape genetics framework. Contrary to our predictions, viviparous populations exhibited greater differentiation and reduced genetic connectivity compared to larviparous populations. Landscape genetic analyses indicate viviparity may be partially responsible for this pattern, as water courses comprised a significant barrier only in viviparous salamanders, probably due to their fully terrestrial life cycle. Agricultural areas and, to a lesser extent, topography also decreased genetic connectivity in both larviparous and viviparous populations. This study is one of very few to explicitly demonstrate the evolution of a derived reproductive mode affects patterns of genetic connectivity. Our findings open avenues for future research to better understand the eco‐evolutionary implications underlying the emergence of terrestrial reproduction in amphibians.

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Fine-scale genetic structure in a salamander with two reproductive modes: Does reproductive mode affect dispersal?

Cited by 18 publications

References 72 publications

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

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

Topography, more than land cover, explains genetic diversity in a Neotropical savanna tree frog

Comparative landscape genetics reveals the evolution of viviparity reduces genetic connectivity in fire salamanders

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