The Role of Python Eggshell Permeability Dynamics in a Respiration‐Hydration Trade‐Off

Abstract

Parental care is taxonomically widespread because it improves developmental conditions and thus fitness of offspring. Although relatively simplistic compared with parental behaviors of other taxa, python egg-brooding behavior exemplifies parental care because it mediates a trade-off between embryonic respiration and hydration. However, because egg brooding increases gas-exchange resistance between embryonic and nest environments and because female pythons do not adjust their brooding behavior in response to the increasing metabolic requirements of developing offspring, python egg brooding imposes hypoxic costs on embryos during the late stages of incubation. We conducted a series of experiments to determine whether eggshells coadapted with brooding behavior to minimize the negative effects of developmental hypoxia. We tested the hypotheses that python eggshells (1) increase permeability over time to accommodate increasing embryonic respiration and (2) exhibit permeability plasticity in response to chronic hypoxia. Over incubation, we serially measured the atomic and structural components of Children's python (Antaresia childreni) eggshells as well as in vivo and in vitro gas exchange across eggshells. In support of our first hypothesis, A. childreni eggshells exhibited a reduced fibrous layer, became more permeable, and facilitated greater gas exchange as incubation progressed. Our second hypothesis was not supported, as incubation O(2) concentration did not affect the shells' permeabilities to O(2) and H(2)O vapor. Our results suggest that python eggshell permeability changes during incubation but that the alterations over time are fixed and independent of environmental conditions. These findings are of broad evolutionary interest because they demonstrate that, even in relatively simple parental-care models, successful parent-offspring relationships depend on adjustments made by both the parent (i.e., egg-brooding behavioral shifts) and the offspring (i.e., changes in eggshell permeability).

The use of ultrasonography to assess reproductive investment and output in pythons

“…Pythons may be under increasing selection to mobilize water into their eggs because their oviposited eggs are highly prone to desiccation and, unlike many other squamates, do not necessarily gain water during incubation (Ackerman & Lott, 2004; Stahlschmidt et al, 2008;Stahlschmidt, Heulin & DeNardo, 2010). Delaying a large proportion of the water investment into eggs until late-stage egg development would shorten the period of potential water stress for gravid females.…”

Dehydration during egg production alters egg composition and yolk immune function

“…Accordingly, we examined the impact of maternal dehydration on reproductive output in the Children's python (Antaresia childreni), which is a capital-breeding, oviparous squamate that has proven to be a valuable study system for examining parent-embryo interactions (e.g., , 2009a,b, 2010, Lorioux et al, 2012, Lourdais et al, 2013.…”

Reduced egg shell permeability affects embryonic development and hatchling traits in Lycodon rufozonatum and Pelodiscus sinensis

“…1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 Hypoxia affects embryonic development 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 the among-species difference in hypoxic responses. Most squamates (lizards and snakes) produce parchment-shelled eggs with high gas permeability (Deeming & Thompson 1991;Packard & DeMarco 1991), and the fibrous layer of parchment-shelled snake eggs decreases during incubation to accommodate the increasing embryonic respiration (Stahlschmidt et al 2010). In contrast, many turtles and all crocodiles produce rigid-shelled eggs with low gas permeability (Thompson 1985;Deeming & Ferguson 1991).…”

“…1the among-species difference in hypoxic responses. Most squamates (lizards and snakes) produce parchment-shelled eggs with high gas permeability (Deeming & Thompson 1991;Packard & DeMarco 1991), and the fibrous layer of parchment-shelled snake eggs decreases during incubation to accommodate the increasing embryonic respiration (Stahlschmidt et al 2010). In contrast, many turtles and all crocodiles produce rigid-shelled eggs with low gas permeability (Thompson 1985;Deeming & Ferguson 1991).…”