Anthropogenic disturbance drives dispersal syndromes, demography, and gene flow in amphibian populations

Abstract

P. L ena. 2020. Anthropogenic disturbance drives dispersal syndromes, demography, and gene flow in amphibian populations. Ecological Monographs 90(2):Abstract. 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, intrapatch 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.

Population position along the fast–slow life‐history continuum predicts intraspecific variation in actuarial senescence

“…By contrast, variation in life-history speed seems to rely on stable demographic F I G U R E 3 Survival probability until a given age in two fast (FAST1 and FAST2) and slow (SLOW1 and SLOW2) populations of Bombina variegata. The predictions on the left of the vertical dashed line correspond to observed ages while those on the right are model projections strategies covarying with behavioural syndromes that likely have genetic bases (Cayuela et al, 2020).…”

“…In addition, as the natural silting of ruts decreases local breeding success over time, individuals frequently disperse to colonize new patches and likely incur energy and mortality costs related to the different stages of the dispersal process (i.e. emigration, transience and immigration; Boualit et al, 2019;Cayuela et al, 2020). By contrast, slow populations occur in non-managed habitats with very limited human activity where dispersal is virtually absent, which likely decrease environmentally driven mortality (Cayuela et al, 2020).…”

“…emigration, transience and immigration; Boualit et al, 2019;Cayuela et al, 2020). By contrast, slow populations occur in non-managed habitats with very limited human activity where dispersal is virtually absent, which likely decrease environmentally driven mortality (Cayuela et al, 2020). Since Williams' (1957) pioneering contribution on this topic, the relationship between environmentally driven mortality and actuarial senescence has been heavily discussed (see Ronget, Garratt, Lemaître, & for reviews).…”

“…Furthermore, changes in dispersal regime within spatially structured populations of B. variegata lead to strong variation in neutral genetic structure. Fast forest populations have a higher genetic diversity, larger effective population size, and higher gene flow between subpopulations than slow riverine populations (Cayuela et al, 2020).…”

“…dispersal syndrome) caused by the high patch turn over resulting from logging operations (Cayuela et al, 2020;Cayuela, Boualit, Arsovski, Bonnaire, Pichenot, et al, 2016). Dispersal is facilitated by a phenotypic specialization that is transgenerationally transmitted: individuals from fast forest populations reared in common garden have a higher boldness and exploration propensity than those from riverine slow populations (Cayuela et al, 2020). The association between high dispersal maintained throughout life span, pre-natally determined behaviour, and accelerated life history (i.e.…”