Energetics meets sexual conflict: The phenology of hibernation in Tasmanian echidnas

Abstract

Echidnas are egg‐laying mammals found across Australia, and in Tasmania they hibernate, resulting in a most unusual mating system: males enter hibernation in late summer–early autumn and arouse in late autumn–early winter to mate, although females are still hibernating. Groups of males compete for matings and both males and females mate with multiple partners. Females that mate early return to hibernation even when pregnant, and males continue to mate with pregnant females. We asked to what extent can the bizarre combination of behavioural and physiological features that characterize reproduction of Tasmanian echidnas be attributed to their phylogeny, and how much is a consequence of their ecology? To understand the interaction between energetics and the echidna mating system in determining the timing of echidna hibernation, we analysed data from an 18‐year study of a wild population of Tasmanian echidnas (Tachyglossus aculeatus setosus) Males in best condition arouse earliest and seek out suitable females, and females that mate early in the mating season re‐enter hibernation while pregnant. Competition between males drives early mating and while mating with males in the best condition could be advantageous for females and their young, egg‐laying in winter is potentially disadvantageous, and post‐mating hibernation by females is a means of delaying hatching of young until environmental conditions are more favourable. This post‐mating hibernation by females is usually disrupted by males which mate with them although they are already pregnant. Comparisons with other echidna populations suggest that a decreased activity period due to hibernation has not increased male–male competition. Similar competition between groups of males for access to females is seen in chlamyphorid armadillos, which occupy a similar ecological niche to echidnas. A free Plain Language Summary can be found within the Supporting Information of this article.

Population demography of the Tasmanian short-beaked echidna (

“…Unlike the majority of mainland echidnas, which show varying degrees of inactivity or torpor, the Tasmanian subspecies (Tachyglossus aculeatus setosus) is an obligate hibernator (Nicol and Andersen 2002). Reproductively mature males enter hibernation in late summer (January-March) and emerge before the winter solstice (May-August) (Nicol et al 2019). They then seek out hibernating females after a three-week sperm maturation period (Morrow et al 2016(Morrow et al , 2017.…”

“…Females enter hibernation later than males (from mid-February to mid-May) and can vary the length of hibernation by several months, with reproductively active females typically emerging from early June, and nonreproducing females in mid-October (Nicol and Andersen 2002). In contrast to males, which emerge spontaneously at a time that depends on their body condition, the majority of reproductively active females emerge from hibernation after being disturbed by males, with males preferring heavier females (Nicol et al 2019). Mating typically occurs from June to September, and egg-laying from July to October (Morrow et al 2009).…”

“…The unusual timing of hibernation in echidnas appears to be a function of their low metabolic rate and long lactation period (Nicol et al 2019): mating must occur in winter for young to be weaned before the following autumn. In Tasmanian echidnas the time from hatching of the young to weaning is about 150 days (Morrow et al 2009); by contrast, the lactation period of Kangaroo Island echidnas, which are not obligate hibernators, is 210 days (Rismiller and McKelvey 2003).…”

“…Due to this pattern of hibernation and reproduction, Tasmanian echidnas could be vulnerable to a warming climate and changes in rainfall pattern: a new analysis of the phenology of hibernation in Tasmanian echidnas (Nicol et al 2019) demonstrates that females have a significantly lower survival than males. One suggestion for this is the delayed timing of prehibernatory fattening in females (mean immergence time 16 March ±16 days) when food supply is less reliable (Nicol and Morrow 2012).…”

Fear of sex: sexual conflict exposed as avoidance in a parthenogenetic invertebrate

“…Generally, it is assumed that males benefit from maximizing such traits like mating frequency; however, females should favor lower mating rates due to the costs of sex (Gavrilets et al 2001). These costs arise from many sources such as increased infection rates from contact with conspecifics (Thrall et al 2000), fitness reducing seminal fluid accessory gland proteins introduced during copulation (Wigby and Chapman 2005), physical damage due to traumatic insemination (Stutt and Siva-Jothy 2001) or due to penile structures that prevent females escaping during copulation (Lange et al 2013), increased energy demands (Nicol et al 2019), and even increased predation risk (Magnhagen 1991).…”