DOI: 10.5061/dryad.q83bk3jdz
title: Anthropogenic disturbance drives dispersal syndromes, demography, and gene flow in amphibian populations

description: 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.
description: <strong>Capture-recapture
 data</strong> We quantified natal and breeding dispersal rates and
 distances in four spatially structured populations (SSP) of
 <em>Bombina variegata</em> (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. <br> 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. <br> The codes used in the capture histories are
 the following:<br> 0: not captured at time t<br> 1: juvenile,
 not captured at time t-1, captured at time t<br> 2: juvenile,
 captured at time t in the same site than at time t-1<br> 3:
 juvenile, captured at time t in a different site than at t-1 located at a
 distance ranging from 100 to 800 m<br> 4: juvenile, captured at time
 t in a different site than at t-1 located at a distance ranging from 800
 to 1500 m<br> 5: juvenile, captured at time t in a different site
 than at t-1 located at a distance longer than 1500 m<br> 6:
 subadult, not captured at time t-1, captured at time t<br> 7:
 subadult, captured at time t in the same site than at time t-1<br>
 8: subadult, captured at time t in a different site than at t-1 located at
 a distance ranging from 100 to 800 m<br> 9: subadult, captured at
 time t in a different site than at t-1 located at a distance ranging from
 800 to 1500 m<br> 10: subadult, captured at time t in a different
 site than at t-1 located at a distance longer than 1500 m<br> 11:
 adult, not captured at time t-1, captured at time t<br> 12: adult,
 captured at time t in the same site than at time t-1<br> 13: adult,
 captured at time t in a different site than at t-1 located at a distance
 ranging from 100 to 800 m<br> 14: adult, captured at time t in a
 different site than at t-1 located at a distance ranging from 800 to 1500
 m<br> 15: adult, captured at time t in a different site than at t-1
 located at a distance longer than 1500 m <strong>Genetic
 data</strong> 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 <em>B. variegata</em>;
 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. <strong>Bibliographic
 references</strong> 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.<br> 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.<br> 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.<br> 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.<br> 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.