Relatedness predicts male mating success in a pond-breeding amphibian

Cayuela, Hugo; Léna, Jean‐Paul; Lengagne, Thierry; Kaufmann, Brigitte; Mondy, Nathalie; Konecny, Lara; Dumet, Adeline; Vienney, Antonin; Joly, Pierre

doi:10.1016/j.anbehav.2017.05.028

Cited by 16 publications

(17 citation statements)

References 80 publications

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“…Controlled mating experiments have shown that females prefer more genetically similar males (Chandler and Zamudio ; Cayuela et al. ), artificial crosses within and between populations have provided evidence for high levels of genetic incompatibility (Sagvik et al. ; Eads et al.…”

Section: Discussionmentioning

confidence: 99%

“…This is not surprising because there is a growing body of evidence to suggest that genetic incompatibility (linked to genetic relatedness) plays a pervasive role in amphibian breeding biology. Controlled mating experiments have shown that females prefer more genetically similar males (Chandler and Zamudio 2008;Cayuela et al 2017), artificial crosses within and between populations have provided evidence for high levels of genetic incompatibility (Sagvik et al 2005;Eads et al 2012), and sperm competition experiments have revealed that males who are more genetically similar to females achieve higher fertilization success (Sherman et al 2008). From an ecological perspective, it is logical to expect a strong role for genetic incompatibility in amphibian breeding because levels of genetic differentiation between amphibian metapopulations (and the potential for local adaptation) are higher than for any other vertebrate class.…”

Section: Discussionmentioning

confidence: 99%

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Genetic benefits of extreme sequential polyandry in a terrestrial‐breeding frog

2019

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Sequential polyandry may evolve as an insurance mechanism to reduce the risk of females choosing mates who are genetically inferior (intrinsic male quality hypothesis) or genetically incompatible (genetic incompatibility hypothesis). The prevalence of such indirect benefits remains controversial, however, because studies estimating the contributions of additive and nonadditive sources of genetic variation to offspring fitness have been limited to a small number of taxonomic groups. Here, we used artificial fertilization techniques combined with a crossclassified breeding design (North Carolina Type II) to simultaneously test the “good genes hypothesis” and the “genetic incompatibility hypothesis” in the brown toadlet (Pseudophryne bibronii); a terrestrial‐breeding species with extreme sequential polyandry. Our results revealed no significant additive or nonadditive genetic effects on fertilization success. Moreover, they revealed no significant additive genetic effects, but highly significant nonadditive genetic effects (sire by dam interaction effects), on hatching success and larval survival to initial and complete metamorphosis. Taken together, these results indicate that offspring viability is significantly influenced by the combination of parental genotypes, and that negative interactions between parental genetic elements manifest during embryonic and larval development. More broadly, our findings provide quantitative genetic evidence that insurance against genetic incompatibility favors the evolution and maintenance of sequential polyandry.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Genetic benefits of extreme sequential polyandry in a terrestrial‐breeding frog

2019

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“…After the third overwintering, individuals are sexually mature (Cayuela et al. , ). Juvenile and adult toads can be individually recognized and surveyed using capture–recapture methods (Cayuela et al.…”

Section: Methodsmentioning

confidence: 99%

“…If they survive, they reach the subadult stage after the second overwintering. After the third overwintering, individuals are sexually mature (Cayuela et al 2017(Cayuela et al , 2018b. Juvenile and adult toads can be individually recognized and surveyed using capture-recapture methods (Cayuela et al 2016b, c).…”

Section: Capture-recapture Surveysmentioning

confidence: 99%

Survival cost to relocation does not reduce population self‐sustainability in an amphibian

Cayuela

Gillet

Laudelout³

et al. 2019

Ecological Applications

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Relocations are increasingly popular among wildlife managers despite often low rates of relocation success in vertebrates. In this context, understanding the influence of extrinsic (e.g., relocation design, habitat characteristics) and intrinsic factors (e.g., age and sex) on demographic parameters, such as survival, that regulate the dynamics of relocated populations is critical to improve relocation protocols and better predict relocation success. We investigated survival in naturally established and relocated populations of yellow‐bellied toads (Bombina variegata), an amphibian that was nearly extinct in Belgium by the late 1980s. We quantified survival at three ontogenetic stages (juvenile, subadult, and adult) in the relocated population, the source population, and a control population. In the relocated population, we quantified survival in captive bred individuals and their locally born descendants. Then, using simulations, we examined how survival cost to relocation affects the self‐sustainability of the relocated population. We showed that survival at juvenile and subadult stages was relatively similar in all populations. In contrast, relocated adult survival was lower than adult survival in the source and control populations. Despite this, offspring of relocated animals (the next generation, regardless of life stage) survived at similar rates to individuals in the source and control populations. Simulations revealed that the relocated population was self‐sustaining under different scenarios and that the fate (e.g., stability or increase) of the simulated populations was highly dependent on the fecundity of relocated adults and their offspring. To summarize, our results indicate that survival in relocated individuals is lower than in non‐relocated individuals but that this cost (i.e., reduced survival) disappears in the second generation. A finer understanding of how relocation affects demographic processes is an important step in improving relocation success of amphibians and other animals.

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“…In pond‐breeding amphibians, these aims are challenging to achieve because adults often emerge only for short periods of time, and because small effective population sizes (Ne) make it difficult to distinguish between older historical events (i.e., at evolutionary timescales) and more recent demographic processes (Dudaniec, Spear, Richardson, & Storfer, ; Johansson, Primmer, & Merilae, ; Titus, Bell, Becker, & Zamudio, ; Wang & Shaffer, ). Another consequence of small effective population sizes within breeding ponds is that each breeding site exhibits high levels of relatedness among individuals (Cayuela et al, ; Funk, Tallmon, & Allendorf, ; Spear, Peterson, Matocq, & Storfer, ; Titus, Bell et al, ; Zamudio & Wieczorek, ). This is especially true in newly formed, or ephemeral ponds, where as few as a single breeding pair may colonize a site, and thus, all individuals may be full or half siblings (Titus, Bell et al, ).…”

Section: Introductionmentioning

confidence: 99%

Sampling related individuals within ponds biases estimates of population structure in a pond‐breeding amphibian

O’Connell

Mulder

Maldonado

et al. 2019

Ecology and Evolution

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Effective conservation and management of pond‐breeding amphibians depends on the accurate estimation of population structure, demographic parameters, and the influence of landscape features on breeding‐site connectivity. Population‐level studies of pond‐breeding amphibians typically sample larval life stages because they are easily captured and can be sampled nondestructively. These studies often identify high levels of relatedness between individuals from the same pond, which can be exacerbated by sampling the larval stage. Yet, the effect of these related individuals on population genetic studies using genomic data is not yet fully understood. Here, we assess the effect of within‐pond relatedness on population and landscape genetic analyses by focusing on the barred tiger salamanders (Ambystoma mavortium) from the Nebraska Sandhills. Utilizing genome‐wide SNPs generated using a double‐digest RADseq approach, we conducted standard population and landscape genetic analyses using datasets with and without siblings. We found that reduced sample sizes influenced parameter estimates more than the inclusion of siblings, but that within‐pond relatedness led to the inference of spurious population structure when analyses depended on allele frequencies. Our landscape genetic analyses also supported different models across datasets depending on the spatial resolution analyzed. We recommend that future studies not only test for relatedness among larval samples but also remove siblings before conducting population or landscape genetic analyses. We also recommend alternative sampling strategies to reduce sampling siblings before sequencing takes place. Biases introduced by unknowingly including siblings can have significant implications for population and landscape genetic analyses, and in turn, for species conservation strategies and outcomes.

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Relatedness predicts male mating success in a pond-breeding amphibian

Cited by 16 publications

References 80 publications

Genetic benefits of extreme sequential polyandry in a terrestrial‐breeding frog

Genetic benefits of extreme sequential polyandry in a terrestrial‐breeding frog

Survival cost to relocation does not reduce population self‐sustainability in an amphibian

Sampling related individuals within ponds biases estimates of population structure in a pond‐breeding amphibian

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