Why being a he/she may help in the race to reproduce.
488 Park Road
Park Orchards, Victoria, 3114, Australia.
Originally published in The Herptile 30(4):139-143.
For the first time ever, this paper reports on an observed behavioral trait of male Death Adders (Acanthophis antarcticus, Acanthophis bottomi, Acanthophis pyrrhus and Acanthophis woolfi) and Tiger Snakes (Notechis scutatus) that may have evolved as a counter or an addition to male/male combat in terms of sexual selection in male snakes.†
In numerous observed cases, two captive male Death Adders have been placed in a cage with a female Death Adder and instead of one or other mating the female, one male is observed mating the other male.
In the first instances this was suspected as aberrant or homosexual behaviour, but based on the frequency of the observation it appears to be common and not genuine homosexual behaviour as interpreted for humans.† Furthermore it appears that the smaller (sub-dominant males) are the ones that usually mimic females (called he/she's in this paper) and allow themselves to be mounted by males.† The evolution of this trait may have conferred some kind of advantage on smaller males over larger ones and hence aided the evolutionary push towards the smaller size of males versus females in some elapids including all Acanthophis species (as listed by Hoser 2002). Further explanation follows in the paper.
INTRODUCTION - THE FIRST OBSERVATIONS
Over many years of keeping Death Adders it was noted that in some cases if two or more reproductively active males were placed with a female, sometimes one male would be observed trying to copulate with the other male instead of the female.
The initial interpretation of this was that it was aberrant homosexual behavior in terms of the males.
However in cases where just one male was placed with a female (either male), the result would be a normal male/female mating.
The situation just described was notable for other reasons as well.
Almost without exception, if a given pair of Death Adders known to engage in such behaviour were introduced together with a female, the same male/male mating response seemed to ensue and in no case would either the roles between the males be reversed or would the subdominant male ever be seen resisting or moving away from the other male trying to mate with it.
In almost all cases, it was the smaller male that allowed itself to be mounted by the larger male.
In my own situation, I had observed this in Acanthophis antarcticus from Sydney, New South Wales, Acanthophis bottomi from Kunnanurra, Western Australia and Acanthophis pyrrhus from north of Port Hedland, Western Australia.
Another keeper, Roy Pails of Ballarat, Victoria, reported the same behavior when he introduced a pair of male Acanthophis woolfi to a female, all from Dajarra, Queensland.
Later when he introduced the males to the female, one at a time, both mounted and mated the female.
In other words, he/she snakes are probably a feature of all Acanthophis species and the lack of observations for the other described species is almost certainly a result of less people keeping them rather than that those species don't engage in such behavior.
At first the trait was thought to be an aberrance related primarily to the captive situation, but this theory took a tumble when it was noted that the same occurred in very large cages where males had the opportunity to get well away from one another.
In other words it appeared to be a deliberate move by one male to fool the other male into mating with it and may have had a parallel in the wild state.
The problem of opportunistically finding a pair of male Death Adders attempting to have sex is huge.† From a practical point of view, finding a single Dearth Adder in the wild isn't easy and to find two in the wild trying to have sex would be nearly impossible.
A CASE IN THE WILD
This didn't involve Death Adders, but rather Tiger Snakes (Notechis scutatus) and is reported here as it indicates that he/she snakes may be far more common than is generally realized among herpetologists.
On 7 February 2003 at 2.30 PM I received a phone call at "Snakebusters" (š‚) from the administration office at the Diamond Creek East Primary School, Diamond Creek, Victoria.
The call was to remove a dangerously venomous Tiger Snake that had been seen going under a large concrete slab adjacent to a playground.
I was able to lift the slab and underneath found a large and very thick-set four foot Tiger Snake (Notechis scutatus) on top of and obviously trying to mate a smaller and much thinner three foot one.
Both Tiger Snakes were males.
In other words, male snakes taking on the role of female snakes is not just something restricted to the captive situation.
WHY DO "HE" SNAKES BECOME "SHE" SNAKES?
The smaller Tiger Snake could have easily fled from the male if he did not want to partake in the sexual overtures from the male.
That he did not is significant and indicated that he/she behavior is a phenomena that occurs in Australian elapids.† Tiger Snakes are also known to be a species to engage in male/male combat, which is generally in relation to breeding activity.
However in terms of my own captive observations of this species and other Australian elapids that engage in male/male combat (including of the genera Cannia, Notechis, Pseudechis and Pseudonaja) the following points are noted.
Combat most often occurs in snakes of similar size.† When there is a strong size disparity, the two snakes will engage in obvious mutual tongue-flicker, with what then appears to be a sort of "stand-off" occurring and the smaller snake ceding right of way to the larger one.
The result is that the smaller snake will move away quickly and only rarely will the larger one bother to pursue it.
In species where male combat is a means to decide who gets to mate, extra size is an evident advantage.
Hence the push for these species to have larger males and males that are generally larger than females.† This is evident in species in the genera Cannia, Notechis, Pseudechis and Pseudonaja.
Acanthophis is relatively unusual among Australian genera of larger elapids in that male/male combat is effectively unknown (Hoser 1995).† Notwithstanding this, it is evident from observations, that larger snakes do as a matter of course get priority of way over smaller ones, even if by virtue of their inherent bulk.† In the rarely observed situations of more than one Death Adder trying to mate with a given female, the larger one will obviously be able to push the smaller one off the female.
As for all snakes, Death Adders are very conscious of one another and in confined spaces (as seen in captivity) will be aware of issues such as size and dominance and will form a sort of social hierarchy generally based on size and gender.
Assuming that size is an advantage in males, even for species that do not engage in male-male combat, then until now, there has been no reasonable explanation for an advantage to be had by smaller males in the mating situation, or at least one that can be used as an explanation for the evolutionary push towards males being smaller in size and smaller than females, save for the general theory that reproductive effort is made proportionately easier in proportionately larger snakes.
Mating in captive (and presumably wild) elapids tends to run a similar course.† Once the male has passed his semen, he will tend to rest for a period ranging from hours to days.
If in a competitive captive situation a subdominant male can fool a dominant one into passing semen either in or on itself, rather than on a female, the subdominant male may then be able to mate with the female himself and hence have an evolutionary advantage.
Hence a potential push towards snakes that become he/she's or perhaps even smaller snakes.
This is particularly so, if it is evident that all (or most) male snakes of a given species such as Death Adders (Acanthophis) have the ability to become he/she's as needed.
My own observations indicate this to be so.
In cages with multiple males, it is relatively uncommon to see two or more males trying to mate a female, but it is not uncommon to see one male trying to mate another.
Hence it seems that males will become he/she's more readily than they will attempt to competitively mount the female snake.
The observation alone indicates that the he/she state is a common one and perhaps far more common in the wild state than has been previously guessed.
Hence we have an explanation for why subdominant (smaller) snakes may be able to have a selection advantage over larger ones and why the evolutionary trend has been towards smaller males in species such as Death Adders.
HE/SHE TIGER SNAKES AND IT'S WIDER MEANING
The observation of a male Tiger Snake allowing itself to take on the role of a female snake is even more significant and not just because it was in the wild state.
Tiger Snakes are known to engage in male/male combat.
Based on the size disparity of the two snakes observed, it appears that the smaller one took on the guise of being a female rather than to engage in a hopeless (losing) combat with a far larger snake.
Generally mature Tiger Snakes are of closer size class, with the two specimens observed being at the upper and lower limits of size in mature snakes.† Hence the observation at Diamond Creek may well have been the exception rather than the norm for the species.
However it does indicate that the ability of snakes to become he/she's may be common to many Australian elapids, but only commonly manifests in species which do not engage in male/male combat.
The fact that the ability of males to mimic females appears to be pre-evolved in most elapids also means that relative size reduction in males of given taxa may have been able to evolve more than once and been dependent on the relative importance of male combat in taxa over long periods, or perhaps vice-versa.
This also makes it possible to infer which species are also most likely to engage in he/she behavior.
Snakes in the genus Pailsus where the females are also the larger sex (like in Acanthophis), are generally known not to engage in male/male combat and hence in the captive situation, it is likely that he/she behavior in males would be seen.
How common he/she behavior is in other groups of snakes is also not known, but it may be far more common than has been suspected so far.†
I am aware of cases of several male snakes being found in a cluster trying to copulate another male in the following widely different species: Diamond Pythons (Morelia spilota) and Australian File Snake (Achrochordus arafurae), with no females being found.
Cases where two or more overwintering and male only Yellow-faced Whipsnakes (Demansia psammophis) or Small-eyed Snakes (Rhinoplocephalus nigrescens) have been found sheltering under the same rock by myself in the Sydney region, or similar cases involving Little-whip Snakes (Unechis flagellum) around Melbourne's north and west may also represent cases where at least one male of the pair or group has adopted the guise of a female in order to waste the reproductive effort of the other/s.
In the case of the first and third species male combat is known, while the non-observation of male combat in Rhinoplocephalus nigrescens could well stem from it's cryptic habits and a lack of specimens in captivity, rather than that the behavior doesn't occur in the species.
Male elapid snakes (and snakes of other families) masquerading as females and enticing other males to mate with them, may not be homosexual as is the context of such behavior as seen in† humans.† He/she snakes are acting in such a manner in order to aid their own chances of mating with a female, including in cases where based on size, the he/she snakes would otherwise be subdominant and perhaps unable to mate with a female if competing by combat or size.
He/she behavior in male snakes is probably quite common both in captivity and in the wild for many species.
Several herpetologists, including those named in this paper who freely shared their observations with me.
Hoser, R. T. 1995. Australiaís Death Adders, Genus Acanthophis, The Reptilian 3 (4) pp. 7-21 and cover, 3 (5):27-34.
Hoser, R. T. 2002 Death Adders (Genus Acanthophis): An Updated overview, including descriptions of 3 New Island species and 2 New Australian subspecies. Crocodilian:Journal of the Victorian Association of Amateur Herpetologists 4(1) September, pages 5-11,16-22,24-30, front and back covers.
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