Among‐individual heterogeneity in maternal behaviour and physiology affects reproductive allocation and offspring life‐history traits in the garter snake <i>Thamnophis elegans</i>

Climate change is generating range shifts in many organisms, notably along the elevational gradient in mountainous environments. However, moving up in elevation exposes organisms to lower oxygen availability, which may reduce the successful reproduction and development of oviparous organisms. To test this possibility in an upwardcolonizing species, we artificially incubated developing embryos of the viperine snake (Natrix maura) using a split-clutch design, in conditions of extreme high elevation (hypoxia at 2877 m above sea level; 72% sea-level equivalent O 2 availability) or low elevation (control group; i.e. normoxia at 436 m above sea level). Hatching success did not differ between the two treatments. Embryos developing at extreme high elevation had higher heart rates and hatched earlier, resulting in hatchlings that were smaller in body size and slower swimmers compared to their siblings incubated at lower elevation. Furthermore, post-hatching reciprocal transplant of juveniles showed that snakes which developed at extreme high elevation, when transferred back to low elevation, did not recover full performance compared to their siblings from the low elevation incubation treatment. These results suggest that incubation at extreme high elevation, including the effects of hypoxia, will not prevent oviparous ectotherms from producing viable young, but may pose significant physiological challenges on developing offspring in ovo. These early-life performance limitations imposed by extreme high elevation could have negative consequences on adult phenotypes, including on fitness-related traits.

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“…2016; Gangloff et al . 2018). However, the long‐term adaptive potential for observed changes in development and physiology has yet to be tested.…”

Section: Discussionmentioning

confidence: 99%

High‐elevation hypoxia impacts perinatal physiology and performance in a potential montane colonizer

et al. 2020

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“…However, factors other than individual identity may explain variation in phenotype expression (e.g. social context, Jolles, Taylor, & Manica, 2016; time between observations, Biro & Stamps, 2015; Gangloff, Sparkman, & Bronikowski, 2018). In such cases, accounting for confounding sources of variation provides an ‘adjusted’ repeatability that more accurately estimates the variance due to individual identity (Dingemanse & Dochtermann, 2014; Nakagawa & Schielzeth, 2010).…”

Section: Introductionmentioning

confidence: 99%

Becoming creatures of habit: Among‐ and within‐individual variation in nesting behaviour shift with age

Delaney

Hoekstra

Janzen

2020

J of Evolutionary Biology

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The quantification of repeatability has enabled behavioural and evolutionary ecologists to assess the heritable potential of traits. For behavioural traits that vary across life, age‐related variation should be accounted for to prevent biasing the microevolutionary estimate of interest. Moreover, to gain a mechanistic understanding of ontogenetic variation in behaviour, among‐ and within‐individual variance should be quantified across life. We leveraged a 30‐year study of painted turtles (Chrysemys picta) to assess how age contributes to variation in the repeatability of nesting behaviours. We found that four components of nesting behaviour were repeatable and that accounting for age increased the repeatability estimate for maternal choice of canopy cover over nests. We detected canalization (diminished within‐individual variance with age) of canopy cover choice in a reduced data set despite no shift in repeatability. Additionally, random regression analysis revealed that females became more divergent from each other in their choice of canopy cover with age. Thus, properly modelling age‐related variance should more precisely estimate heritable potential, and assessing among‐ and within‐individual variance components in addition to repeatability will offer a more mechanistic understanding of behavioural variation across age.

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“…4). This shows that (meta-)population variability shifts in the directions anticipated from ecological theory when spatial individual heterogeneity in metapopulation dynamics is removed (Vindenes, Engen, and Sæther 2008; Gangloff, Sparkman, and Bronikowski 2018; Hamel et al 2018; Smallegange, Fernandes, and Croll 2018). Disrupting spatial phenotypic heterogeneity through randomization decreases in consequence both population sizes and their variability across the connectedness gradient.…”

Section: Discussionmentioning

confidence: 71%

Individual heterogeneity and its importance for metapopulation dynamics

Masier

Dahirel

Mortier

et al. 2020

Preprint

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Habitat fragmentation reduces the area of habitat patches and their connectedness in the landscape. It is well established that the level of connectedness impacts connectivity and metapopulation dynamics, and is therefore a central tenet in conservation biology. Connectedness equally generates sorting of phenotypes within the spatial network and therefore impacts local and regional eco-evolutionary dynamics. Paradoxically, recommendations for species conservation rely on principles derived from theory that neglects any individual phenotypic heterogenety and spatial organization.By creating experimental metapopulations using the model species Tetranychus urticae (two-spotted spider mite) with three levels of landscape connectedness and by regularly removing phenotypic structure in a subset of these populations, we tested the degree to which regional and local population dynamics are determined both by network connectedness and the phenotypic spatial organization.Our results show that some aspects of metapopulation dynamics can be attributed to the evolution of dispersal. More importantly, we find self-organization of phenotypic spatial structure to equalize the effects of reduced connectedness on metapopulation dynamics. These changes were all in the direction of improved metapopulation persistence. Contrary to expectations, the most connected local patches showed an overall reduced local population size, possibly originating from a faster depletion of resources from immigrants or transiting individuals.This experiment shows how metapopulation dynamics can significantly deviate from theoretical expectations if individual heterogeneity is considered, and more importantly that disruption of this phenotypic self-structuring may drive metapopulation dynamics towards higher risks of extinction.Significance StatementChanges in connectedness impact metapopulation dynamics but also the spatial organization of individual phenotypic heterogeneity. The extent to which metapopulation dynamics depend on this phenotypic structuring is unknown, despite the fact metapopulation theory is at the heart of conservation biology. By using experimental metapopulations and a randomization treatment, we demonstrate that the emerging spatial organization of individuals (both genetically and phenotypically) is a major driver of metapopulation dynamics. This spatial organization may be important as it may equalize all variation in metapopulation dynamics across a gradient of connectivity. This potentially rescuing effect stemming from the self-organization of phenotypes in metapopulations is of uttermost importance for conservation and translocation actions.

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Among‐individual heterogeneity in maternal behaviour and physiology affects reproductive allocation and offspring life‐history traits in the garter snake Thamnophis elegans

Cited by 20 publications

References 113 publications

High‐elevation hypoxia impacts perinatal physiology and performance in a potential montane colonizer

High‐elevation hypoxia impacts perinatal physiology and performance in a potential montane colonizer

Becoming creatures of habit: Among‐ and within‐individual variation in nesting behaviour shift with age

Individual heterogeneity and its importance for metapopulation dynamics

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