There is growing evidence that anthropogenic landscapes can strongly influence the evolution of dispersal, particularly through fragmentation, and may drive organisms into an evolutionary trap by suppressing dispersal. However, the influence on dispersal evolution of anthropogenic variation in habitat patch turnover has so far been largely overlooked. In this study, we examined how human-driven variation in patch persistence affects dispersal rates and distances, determines dispersal-related phenotypic specialization, and drives neutral genetic structure in spatially structured populations. We addressed this issue in an amphibian, Bombina variegata, using an integrative approach combining capture-recapture modeling, demographic simulation, common garden experiments, and population genetics. B. variegata reproduces in small ponds that occur either in habitat patches that are persistent (i.e. several decades or more), located in riverine environments with negligible human activity, or in patches that are highly temporary (i.e. a few years), created by logging operations in intensively harvested woodland. Our capture-recapture models revealed that natal and breeding dispersal rates and distances were drastically higher in spatially structured populations (SSPs) in logging environments than in riverine SSPs. Population simulations additionally showed that dispersal costs and benefits drive the fate of logging SSPs, which cannot persist without dispersal. The common garden experiments revealed that toadlets reared in laboratory conditions have morphological and behavioral specialization that depends on their habitat of origin. Toadlets from logging SSPs were found to have higher boldness and exploration propensity than those from riverine SSPs, indicating transgenerationally transmitted dispersal syndromes. We also found contrasting patterns of neutral genetic diversity and gene flow in riverine and logging SSPs, with genetic diversity and effective population size considerably higher in logging than in riverine SSPs. In parallel, intra-patch inbreeding and relatedness levels were lower in logging SSPs. Controlling for the effect of genetic drift and landscape connectivity, gene flow was found to be higher in logging than in riverine SSPs. Taken together, these results indicate that anthropogenic variation in habitat patch turnover may have an effect at least as important as landscape fragmentation on dispersal evolution and the long-term viability and genetic structure of wild populations.

Capture-recapture data

We quantified natal and breeding dispersal rates and distances in four spatially structured populations (SSP) of Bombina variegata (L1, L2 and R1, R2) for which breeding rate dispersal had been previously estimated (Cayuela et al. 2016a, 2016b). A detailed description of the four SSPs can also be found in two previous studies (Cayuela et al. 2016a, 2016b). The number of patches (defined as a group of ruts or ponds) occupied by each SSP ranged from 8 to 189. The two logging SSPs were exhaustively surveyed (i.e., captures were performed within all patches present in the study area) to detect long-distance dispersal events and to obtain unbiased dispersal kernels.

Each SSP was monitored for a period of at least five years in one to five capture sessions per year that were usually between two weeks to one month apart. At each capture session, all the patches were sampled in the daytime and toads were captured by hand or dipnet. Based on previous studies (Cayuela et al. 2016a, 2016c), we considered three life stages: juveniles (i.e. post-wintering metamorphs), subadults (two-year-old immature animals) and adults (i.e. breeders, three years old or more). We identified each individual by the specific pattern of black and yellow mottles on its belly, recorded by photographs. Multiple comparisons of patterns were performed using a robust computing tool (Extract Compare) to minimize misidentification errors (Hiby & Lovell 1990). This resulted in a total dataset of 12,721 individual CR histories.

The codes used in the capture histories are the following:
0: not captured at time t
1: juvenile, not captured at time t-1, captured at time t
2: juvenile, captured at time t in the same site than at time t-1
3: juvenile, captured at time t in a different site than at t-1 located at a distance ranging from 100 to 800 m
4: juvenile, captured at time t in a different site than at t-1 located at a distance ranging from 800 to 1500 m
5: juvenile, captured at time t in a different site than at t-1 located at a distance longer than 1500 m
6: subadult, not captured at time t-1, captured at time t
7: subadult, captured at time t in the same site than at time t-1
8: subadult, captured at time t in a different site than at t-1 located at a distance ranging from 100 to 800 m
9: subadult, captured at time t in a different site than at t-1 located at a distance ranging from 800 to 1500 m
10: subadult, captured at time t in a different site than at t-1 located at a distance longer than 1500 m
11: adult, not captured at time t-1, captured at time t
12: adult, captured at time t in the same site than at time t-1
13: adult, captured at time t in a different site than at t-1 located at a distance ranging from 100 to 800 m
14: adult, captured at time t in a different site than at t-1 located at a distance ranging from 800 to 1500 m
15: adult, captured at time t in a different site than at t-1 located at a distance longer than 1500 m

Genetic data

We examined neutral genetic variations within two SSPs in riverine environments (R1 and R2) and two SSPs in logging environments (L3 and L4) using 15 polymorphic microsatellite markers (described and tested in Cayuela et al. 2017). The four SSPs were selected according to the following criteria: (1) SSPs embedded in a relatively continuous forested matrix to avoid any confounding effect of matrix composition on gene flow – woodland is generally considered highly favorable for the movement of forest amphibians such as B. variegata; and (2) two small (R1 and L3) and two large SSPs (R2 and L4) to control for genetic drift. The number of patches and DNA sampled per SSP are given in given in the original paper published in Ecological Monographs. We used the protocol described in Cayuela et al. (2017) for DNA extraction and amplification, individual genotyping, and allele scoring.

Bibliographic references

Cayuela, H., Arsovski, D., Thirion, J. M., Bonnaire, E., Pichenot, J., Boitaud, S., Brison, A.-L., Miaud, C., Joly, P., & Besnard, A. (2016a). Contrasting patterns of environmental fluctuation contribute to divergent life histories among amphibian populations. Ecology, 97, 980-991.
Cayuela, H., Boualit, L., Arsovski, D., Bonnaire, E., Pichenot, J., Bellec, A., Miaud, C., Léna, J.-P., Joly, P., & Besnard, A. (2016b). Does habitat unpredictability promote the evolution of a colonizer syndrome in amphibian metapopulations?. Ecology, 97, 2658-2670.
Cayuela, H., Arsovski, D., Thirion, J. M., Bonnaire, E., Pichenot, J., Boitaud, S., Miaud, C., Joly, P., & Besnard, A. (2016c). Demographic responses to weather fluctuations are context dependent in a long‐lived amphibian. Global Change Biology, 22, 2676-2687.
Cayuela, H., Léna, J. P., Lengagne, T., Kaufmann, B., Mondy, N., Konecny, L., Dumet, A., Vienney, A., & Joly, P. (2017). Relatedness predicts male mating success in a pond-breeding amphibian. Animal Behaviour, 130, 251-261.
Hiby, L., & Lovell, P. (1990). Computer-aided matching of natural markings: a prototype system for grey seals. Report of the International Whaling Commission, 12, 57–61.