Please consider this as my critical assessment of the manuscript entitled “Sexes in sync: phenotypic plasticity and sexual selection maintain phenological synchrony between the sexes in a wild hibernator” submitted to the Proceedings of the Royal Society B by Thompson et al. In this contribution, the authors detail findings of a 27 year investigation of sex specific phenology of ending torpor and emergence from hibernation of free-living Columbian ground squirrels (Urocitellus columbianus). They found that the phenology of end of torpor and subsequent emergence of males and females displayed similar plasticity in response to springtime environmental conditions and thus sexes have remained synchronized over the 27-year study and should remain so into the future. I found this study compelling and well conducted, analyzed and written. That the authors present results that differ significantly from what has been published for the closely related arctic ground squirrel is most intriguing. I include below, minor and specific comments and questions for the authors. Further, I ask that the authors expand upon the likely reasons for the differences in vernal timing between the arctic and the Columbian ground squirrels.
Ln 53: What are these few studies that have demonstrated desynchronizations between the sexes? Please add needed citations.
Ln 80 and throughout: Arctic used as an adjective as in arctic ground squirrel should be lower case.
Ln 81: In this study of arctic ground squirrels, it is important to note that not all males failed to delay ending heterothermy and emergence in spring. This was only true for reproductive males. Non-reproductive males exhibited similar delays as did females in response to prolonged snow-cover.
Ln 84: Change to plural form "hibernacula".
Ln 111: Arguably, this is true for most if not all mammals, and not just hibernators. Please see and add Hau et al. (2017).
Hau, et al. (2017) Timing as a sexually selected trait: the right mate at the right moment. Philosophical Transactions of the Royal Society, B. 372(1734). DOI: 10.1098/rstb.2016-0249
Ln 134-135: Please provide details of these estimators. Does timing of appearance in the population refer to the timing of emergence in spring?
Ln 216: What proportion of the animals were considered reproductively immature? How was this determined? If the data exist, it would be interesting to see average and year to year differences in the proportion of male that fail to attain reproductive maturity following their first hibernation.
Ln 383-385: I think it is important to note here that the environmental conditions experienced by males when they "elect" to end heterothermy and then "elect" to resume surface activity are likely quite different between the study sites of the Columbian ground squirrel (this study) and that reported for the arctic ground squirrel. When male arctic ground squirrels end heterothermy in March in the Arctic, ambient air temperatures are well below zero and soil temperatures are at their annual minima. Moreover, at this time and even when arctic ground squirrels emerge from hibernation, there is typically 100% snow-cover and green-up is still 4 to 6 weeks away. Yet, even under winter-like conditions, both male and female arctic ground squirrels end heterothermy and emerge. This early emergence relative to environmental conditions is essential to ensure sufficient time for offspring to grow, develop and fatten sufficiently to survive hibernation.
This requires that males secure a cache in late summer and draw from that resource to fuel their 3 weeks of reproductive development. There appears to be no temperature cue that they can rely upon to time the end of heterothermy and they are a meter below the ground that is overlain with a blanket of snow--no light cues or significant air exchange. Because reproductive maturation is a fixed duration, and because they have no apparent cues that signal current surface conditions or that predict conditions some 21 days out, it seems that they have evolved to rely heavily on the signaling of time from a central circannual oscillator to time their end of heterothermy and emergence from hibernation.
Ln 430-432: A recently published long-term study of arctic ground squirrels should be cited here along with the Williams et al. 2017 paper. Williams et al., 2017 shows an acute responsiveness of female arctic ground squirrels to late season snow events. However, the new paper (Chmura et al., 2023) shows a long term and significant trend in earlier termination of hibernation and emergence of arctic ground squirrel females (but not males) over a couple of decades of warming soils in the Arctic.
Chmura et al., (2023) Climate change is altering the physiology and phenology of an arctic hibernator. Science. Vol 380, Issue 6647, pp. 846-849 DOI: 10.1126/science.adf5341
Collectively, the findings in this paper on phenology of Columbian ground squirrels and those on arctic ground squirrel phenology indicate very different responses (among males of the species at least) that should be explored as deeply as is possible.