Reproduction in Changing Environments
(C) Geoff While
Anthropogenic environmental changes are causing dramatic shifts in the spatial and temporal arrangement of organisms and their behavior, with important ramifications for mating and social systems. Research in the Moss lab aims to generate both a theoretical and empirical foundation from which to explore these outcomes.
Disentangling the ecological drivers of sex variation in thermal plasticity
For most animals, males and females achieve reproductive success through distinct developmental, physiological, and behavioral adaptations, which may favor different strategies for coping with thermal variation. Current work in the Moss Lab leverages a locally abundant and experimentally tractable species, Plethodon cinereus, to study the links between thermal plasticity at the individual level, sex-specific reproductive strategies and outcomes, and selection on male and female traits. To accomplish this, we are taking a hypothesis-driven approach which combines comparative physiology, behavioral ecology, and ground-truthing in natural populations.
Comparative physiology
Thermal acclimation experiments can reveal valuable details about an organisms’ capacity to maintain energy balance and perform key functions across a range of environmental conditions. For lungless salamanders, the primary mechanism of physiological acclimation is to alter the permeability of their skin, which conserves water and energy at the cost of restricted oxygen uptake for energetically demanding activities, such as foraging and mating.
Using automated respirometry methods, our research group is revealing important differences in thermal acclimation strategies among sexes and reproductive classes in eastern red-backed salamanders. Ongoing and future experiments aim to deepen mechanistic understanding of these sex differences; for example, investigating whether sexually dimorphic acclimation strategies are underpinned by heightened hydric costs of egg production
Figure 1: Standard metabolic rate (mass-adjusted VO2, in ul/hr) measured at 16*C in three classes of salamanders following three weeks of thermal acclimation at one of two treatments (Cool or Warm) in the spring: gravid females (N=14 cool, N=14 warm), non-gravid females (N=14 cool, N=13 warm), and males (N=14 cool, N=14 warm).
Related projects are exploring the impacts of sexually dimorphic thermal acclimation strategies on locomotor performance.
Left: Natalie Nazemie, an undergraduate researcher in the Moss Lab, patiently coaches a salamander through its physical endurance trial on a mechanized treadmill.
Above: Evaporative water loss traces recorded using flow-through respirometry.
Behavioral ecology
Understanding how animals modify behavior across thermal environments is critical to making accurate predictions about the impact of climate on demographic processes. Plethodontids are semi-fossorial and, due to exceptionally low metabolic rates, they are capable of retreating underground for days or even months at a time to escape suboptimal conditions
The Moss Lab is combining thermal manipulation experiments in the field and lab to better understand how sex-specific strategies for coping with thermal variation could translate into variation in surface activity throughout the active season.
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Above: Soil microcosms designed to replicate subterranean thermal and hydric gradients to observe salamander thermoregulatory behaviors.
Left: Bella Badon, a RaMP researcher hosted in the Moss Lab, scans for surface-active salamanders during the nocturnal activity window as part of an outdoor mesocosm experiment.
Ground-truthing
A promising avenue for investigating the ecological drivers of sex variation in thermal plasticity is to exploit natural variation in sex-specific reproductive costs and strategies across populations. For example, in ectotherms, female-biased sexual size dimorphism (SSD) tends to be more exaggerated in populations living below their thermal limit (Fig. 2), reflecting stronger fecundity selection relative to male sexual selection in highly seasonal environments
Partnering with the Salamander Population and Adaptation Research Collaboration network (SPARCnet), the Moss lab is working to generate long-term natural population datasets spanning an elevational gradient in southwest VA which will allow us to ground-truth predictions borne out of comparative physiology and behavioral ecology experiments in response to natural climatic variation.
For more information about our long-term monitoring initiative, see the Field Study page!
Figure 2: Population differences across our study sites, showing mean daily temperature profiles averaged over the last five years (top) and patterns of sexual-size dimorphism, determined by comparing snout-vent lengths (SVL) of adult males and gravid females sampled in Fall 2024 (bottom). Colors indicate temperatures above (in red) and below (in blue) thermal limits for activity.
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Thermal effects on reproductive traits
An individual’s reproductive success is constrained by the outcomes of courtship interactions, the performance of which is influenced by a myriad of biotic and abiotic variables. Because both the performance and evaluation of courtship are typically costly, variable thermal environments may select for heightened short-term behavioral plasticity to ensure that pre-copulatory investments align with the occurrence of optimal thermal conditions.
A complementary approach to studying short-term plasticity in reproductive behaviors is to examine changes in proximate mechanisms. Steroid hormones play a critical role in regulating sexual behaviors and also act to prime individuals for energetically intensive activities, such as courtship behavior. However, it is currently unknown whether salamanders exhibit plasticity in either courtship behaviors or endocrine responses when faced with short-term temperature fluctuations that may arise unexpectedly and transiently throughout a breeding season. To explore this possibility, we will utilize local populations of Desmognathus ochrophaeus salamanders. We will also take advantage of some fascinating aspects of this species' biology, such as long-term sperm storage, to explore the consequences of warming winters on post-copulatory sexual selection.
Previous Work
(C) M. Kartje
Reproductive ecology and conservation
Jen's dissertation research examined the impact of human habitation on demographic and evolutionary potentials of a critically endangered lizard, the Sister Islands Rock Iguana. Through a combination of mark-recapture surveys, nest excavations, drone-assisted radio telemetry, and genetic analysis, this work revealed synergistic effects of natal microenvironment and inbreeding level on offspring performance.
A second key outcome was that female mating and nesting​ strategies that shape conditions for developing embryos depend on social conditions experienced during the reproductive season. Thus, the key to understanding the repercussions of human land use for the most vulnerable age classes lies in understanding its effects on distributions and interactions among adults.
Temperature-mediated mating rates
As an Endeavour Postdoctoral Fellow at the University of Tasmania, Australia, Jen collaborated with Dr. Geoff While to develop a framework for studying how the thermal environment may mediate social transformations at various evolutionary stages. In an ambitious experiment involving lizards (Liopholis whitii) and semi-natural mesocosms, the team then went about testing these ideas by manipulating the thermal conditions experienced by replicated populations over the course of the breeding season. Their prediction was that warmer temperatures would promote higher activity (because Tasmania is temperate and spring are typically cooler) which would allow for higher rates of mating and, ultimately, shifts in the strength and targets of sexual selection. What they instead found was that more restrictive thermal regimes subject activity to stronger fecundity selection on females, but not sexual selection on males (Fig 3).
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Figure 3: (A) Replicated outdoor mesocosms used to manipulate thermal conditions, demonstrating temperature-dependent shifts in fecundity (B) and sexual selection (C) on individual activity.
Because reproductive outcomes for males and females are inextricably linked, this suggests that underlying sex differences may constrain the ability of a population to respond to temperature even after accounting for behavioral plasticity at the individual level.