The quantitative genetic basis of adaptive divergence in the moor frog (Rana arvalis) and its implications for gene flow

Environmental change can simultaneously cause abiotic stress and alter biological communities, yet adaptation of natural populations to co-changing environmental factors is poorly understood. We studied adaptation to acid and predator stress in six moor frog ( Rana arvalis ) populations along an acidification gradient, where abundance of invertebrate predators increases with increasing acidity of R. arvalis breeding ponds. First, we quantified divergence among the populations in anti-predator traits (behaviour and morphology) at different rearing conditions in the laboratory (factorial combinations of acid or neutral pH and the presence or the absence of a caged predator). Second, we evaluated relative fitness (survival) of the populations by exposing tadpoles from the different rearing conditions to predation by free-ranging dragonfly larvae. We found that morphological defences (relative tail depth) as well as survival of tadpoles under predation increased with increasing pond acidity (under most experimental conditions). Tail depth and larval size mediated survival differences among populations, but the contribution of trait divergence to survival was strongly dependent on prior rearing conditions. Our results indicate that R. arvalis populations are adapted to the elevated predator pressure in acidified ponds and emphasize the importance of multifarious selection via both direct (here: pH) and indirect (here: predators) environmental changes.

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ADAPTIVE DIVERGENCE IN MOOR FROG (RANA ARVALIS) POPULATIONS ALONG AN ACIDIFICATION GRADIENT: INFERENCES FROMQST-FSTCORRELATIONS

Evolution ◽

10.1111/j.1558-5646.2011.01472.x ◽

2011 ◽

Vol 66 (3) ◽

pp. 867-881 ◽

Cited By ~ 37

Author(s):

Sandra Hangartner ◽

Anssi Laurila ◽

Katja Räsänen

Keyword(s):

Adaptive Divergence ◽

Rana Arvalis ◽

Moor Frog

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De novo oviduct transcriptome of the moor frog Rana arvalis: a quest for maternal effect candidate genes

PeerJ ◽

10.7717/peerj.5452 ◽

2018 ◽

Vol 6 ◽

pp. e5452

Author(s):

Longfei Shu ◽

Jie Qiu ◽

Katja Räsänen

Keyword(s):

Candidate Genes ◽

Maternal Effects ◽

De Novo ◽

Full Range ◽

Natural Populations ◽

Population Variation ◽

Adaptive Divergence ◽

Rana Arvalis ◽

Egg Jelly ◽

Moor Frog

Maternal effects can substantially affect ecological and evolutionary processes in natural populations. However, as they often are environmentally induced, establishing their genetic basis is challenging. One important, but largely neglected, source of maternal effects are egg coats (i.e., the maternally derived extracellular matrix that surrounds the embryo). In the moor frog, the gelatinous egg coats (i.e., egg jelly) are produced in the mother’s oviduct and consist primarily of highly glycosylated mucin type O-glycans. These O-glycans affect jelly water balance and, subsequently, contribute to adaptive divergence in embryonic acid tolerance. To identify candidate genes for maternal effects, we conducted RNAseq transcriptomics on oviduct samples from seven R. arvalis females, representing the full range of within and among population variation in embryonic acid stress tolerance across our study populations. De novo sequencing of these oviduct transcriptomes detected 124,071 unigenes and functional annotation analyses identified a total of 57,839 unigenes, of which several identified genes likely code for variation in egg jelly coats. These belonged to two main groups: mucin type core protein genes and five different types of glycosylation genes. We further predict 26,711 gene-linked microsatellite (simple sequence repeats) and 231,274 single nucleotide polymorphisms. Our study provides the first set of genomic resources for R. arvalis, an emerging model system for the study of ecology and evolution in natural populations, and gives insight into the genetic architecture of egg coat mediated maternal effects.

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Maternally determined adaptation to acidity in Rana arvalis: Are laboratory and field estimates of embryonic stress tolerance congruent?

Canadian Journal of Zoology ◽

10.1139/z07-064 ◽

2007 ◽

Vol 85 (7) ◽

pp. 832-838 ◽

Cited By ~ 11

Author(s):

M. Persson ◽

K. Räsänen ◽

A. Laurila ◽

J. Merilä

Keyword(s):

Stress Tolerance ◽

Local Adaptation ◽

Laboratory Experiments ◽

Genetic Basis ◽

Laboratory Finding ◽

Acid Stress ◽

Population Variation ◽

Rana Arvalis ◽

Quantitative Genetic ◽

In The Wild

Geographic variation indicating local adaptation, as well as its quantitative genetic basis, is commonly investigated in common garden experiments in the laboratory. However, the applicability of laboratory results to the complex conditions experienced by populations in the wild may be limited. Our previous laboratory experiments showed maternally determined local adaptation in embryonic acid-stress tolerance (viz. survival) of the moor frog, Rana arvalis Nilsson, 1842. Here we tested whether this laboratory finding holds even when embryos are exposed to acid stress in the wild. We conducted reciprocal crosses between an acid-origin population and a neutral-origin population of R. arvalis and transplanted the embryos to an acid site (pH ~4) in the field. Embryonic survival was much lower in the field experiment than in previous laboratory experiments, but, consistent with laboratory work, embryos from acid-origin females had threefold higher survival than embryos from neutral-origin females. These results suggest that laboratory tests can provide appropriate estimates of among population variation, as well as the quantitative genetic basis of acid-stress tolerance in amphibians.

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Adaptive divergence of the moor frog (Rana arvalis) along an acidification gradient

BMC Evolutionary Biology ◽

10.1186/1471-2148-11-366 ◽

2011 ◽

Vol 11 (1) ◽

pp. 366 ◽

Cited By ~ 23

Author(s):

Sandra Hangartner ◽

Anssi Laurila ◽

Katja Rasanen

Keyword(s):

Adaptive Divergence ◽

Rana Arvalis ◽

Moor Frog

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An Overview of the Helminths of Moor Frog Rana arvalis Nilsson, 1842 (Amphibia: Anura) in the Volga Basin

Diversity ◽

10.3390/d13020061 ◽

2021 ◽

Vol 13 (2) ◽

pp. 61

Author(s):

Igor V. Chikhlyaev ◽

Alexander B. Ruchin

Keyword(s):

Systematic Position ◽

Helminth Fauna ◽

Helminth Species ◽

Volga Basin ◽

Rana Arvalis ◽

Amphibian Species ◽

Volga River ◽

Spirometra Erinacei ◽

First Time ◽

Moor Frog

This is the first review of the helminth fauna of the moor frog Rana arvalis Nilsson, 1842 from the Volga river basin (Russia). The article summarizes the authors’ and literature data on the helminthic fauna of this species. The method of complete helminthological dissection was used. Thirthy-eight helminth species were recorded from three classes: Cestoda (1), Trematoda (28), and Chromadorea (9). Nine helminth species are new to the moor frog in Russia: trematodes Gorgodera varsoviensis Sinitzin, 1905, Strigea falconis Szidat, 1928, larvae, Neodiplostomum spathoides Dubois, 1937, larvae, Tylodelphys excavata (Rudolphi, 1803), larvae, Pharyngostomum cordatum (Diesing, 1850), larvae, Astiotrema monticelli Stossich, 1904, larvae and Encyclometra colubrimurorum (Rudolphi, 1819), larvae, nematodes Strongyloides spiralis Grabda-Kazubska, 1978 and Icosiella neglecta (Diesing, 1851). The cestode Spirometra erinacei (Rudolphi, 1918), larvae were observed of this amphibian species in the Volga basin for the first time. The nematodes Rhabdias bufonis, Oswaldocruzia filiformis, Cosmocerca ornata and the trematode Haplometra cylindracea form the core of the helminth fauna of the moor frog. Information on species of helminths includes systematic position, localization, areas of detection, type and scheme of life cycle, geographical distribution, and degree of specificity to host amphibians.

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Adaptive Divergence under Gene Flow along an Environmental Gradient in Two Coexisting Stickleback Species

Genes ◽

10.3390/genes12030435 ◽

2021 ◽

Vol 12 (3) ◽

pp. 435

Author(s):

Thijs M. P. Bal ◽

Alejandro Llanos-Garrido ◽

Anurag Chaturvedi ◽

Io Verdonck ◽

Bart Hellemans ◽

...

Keyword(s):

Gene Flow ◽

Brackish Water ◽

Environmental Gradient ◽

Spatial Scales ◽

Morphological Differentiation ◽

Genotyping By Sequencing ◽

Adaptive Divergence ◽

Linkage Groups ◽

Closely Related Species ◽

Genomic Patterns

There is a general and solid theoretical framework to explain how the interplay between natural selection and gene flow affects local adaptation. Yet, to what extent coexisting closely related species evolve collectively or show distinctive evolutionary responses remains a fundamental question. To address this, we studied the population genetic structure and morphological differentiation of sympatric three-spined and nine-spined stickleback. We conducted genotyping-by-sequencing and morphological trait characterisation using 24 individuals of each species from four lowland brackish water (LBW), four lowland freshwater (LFW) and three upland freshwater (UFW) sites in Belgium and the Netherlands. This combination of sites allowed us to contrast populations from isolated but environmentally similar locations (LFW vs. UFW), isolated but environmentally heterogeneous locations (LBW vs. UFW), and well-connected but environmentally heterogenous locations (LBW vs. LFW). Overall, both species showed comparable levels of genetic diversity and neutral genetic differentiation. However, for all three spatial scales, signatures of morphological and genomic adaptive divergence were substantially stronger among populations of the three-spined stickleback than among populations of the nine-spined stickleback. Furthermore, most outlier SNPs in the two species were associated with local freshwater sites. The few outlier SNPs that were associated with the split between brackish water and freshwater populations were located on one linkage group in three-spined stickleback and two linkage groups in nine-spined stickleback. We conclude that while both species show congruent evolutionary and genomic patterns of divergent selection, both species differ in the magnitude of their response to selection regardless of the geographical and environmental context.

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