Lovers and fighters, and the difficulties of understanding their coexistence

by Isabel Smallegange, who acknowledges the DynaMite team, currently comprising Kat Stewart and Flor Rhebergen, for insightful discussions.

Sexual selection theory aims to understand the exaggerated traits of males within the context of mating

The most cited example of exaggerated male traits is that of the tail feathers of male peacocks: they are an absolute hindrance to fly with and thus to escape from predators. So why do males still have these extravagant tail feathers? Because, if they are alive, this signals to females that they must be in great condition if, despite these cumbersome tail feathers, they can stay alive (escape predation). In a nut shell, these females then develop a preference to mate with the males with the most extravagant tail feathers, and then produce sons with extravagant tail feathers.


Sometimes, it is not female choice that drives the evolution of exaggerated traits, but male-male competition. Think of the antlers of males of many deer species. In the mating season, they are used as weapons to defend and monopolise a herd of hinds to secure reproductive success. My study species, the bulb mite (Rhizoglyphus robini), has been used to understand the evolution of such male weapons. Male adult bulb mites are fighters or scramblers: fighters possess weapons (thick muscular legs with sharp ends that can be used to kill conspecifics), whereas scramblers are defenceless. It is clear why the bulb mite male weaponry can be advantageous. But what is the advantage of being a scrambler? Why can both male morphs coexist?

Nuptial gifts

The first idea was that they are merely making ‘the best of a bad job’: scramblers are the ‘losers’ that cannot develop the energetically costly fighter legs (Radwan 2009). But sexual selection theory offers another explanation. In some species, males offer potential mates a nuptial gift: a piece of food to eat in order to distract the female so that the male can mate, or which provides an energy source for offspring production after mating. In some species, the nuptial gift is the male himself – a process referred to as sexual cannibalism.

My former PhD student, Tom van den Beuken, set out in his thesis to test the hypothesis that, in the bulb mite, scramblers can have an advantage over fighters if they have sufficient energy resources available to provide the female with a nuptial gift in the form of excess sperm or another nutritious fluid that the male transfers during mating. The assumption was that fighters would not be able to do so, because they have to spend energy maintaining these big muscular fighter legs. In a recent paper (Van den Beuken & Smallegange 2018), Tom presents his findings that suggest that male bulb mites can transfer such nuptial gifts, as females that had mated with males that had fed recently produced more eggs than if their mates had been starved. He also found that females increased in mass, but males decreased in mass over the course of the experiment. From these observations we inferred that fed males are able to transfer nutrients, a nuptial gift, to their mate. Crucially though, we did not find a difference between whether or not a female’s mate was a fighter or scrambler. Males of both morphs therefore appeared to be able to transfer nuptial gifts.

Tom next repeated the experiment (Van den Beuken et al. 2019), but this time allowed the males to mate repeatedly to assess if fighters and scramblers differed in how many eggs their mates produced after a male had mated once, twice or three times. Most eggs were produced after the first mating. Importantly, Tom found that, regardless of whether males were starved or fed, females that had mated to scramblers always produced more eggs than females mated to fighters.

Do we now know why fighters and scramblers can coexist in the same population?

No, we don’t. For both morphs to be able to coexist, neither morph should always perform best. What we know so far is that fighters will always outcompete scramblers in fights as they have their fighter legs with which they can kill scramblers, whereas scramblers are defenceless. This means that fighters are able to prevent scramblers from gaining access to females to mate. On the other hand, if scramblers have secured a mate, the female they mate with will likely lay more eggs then when mated to a fighter. But we have not identified exactly under what circumstances scramblers do better in the mating arena than fighters, and under what circumstances fighters do better than scramblers, and how these circumstances vary over time for bulb mite populations to have the conditions under which both morphs can coexist.

Is there another hypothesis to explain male morph coexistence?

Yes, there is. Perhaps the reason for why fighters and scramblers coexist does not lie in whoever performs best in the mating arena, but is instead explained by the somatic state of a male at the moment of maturation. Specifically, it could be physiologically too expensive for bad-condition males to sustain prioritised physiological processes, such as somatic maintenance and development, and also produce fighter morphology. Such poor-condition males can refrain from developing fighter morphology and instead redirect resources to prioritized, physiological processes to recover somatic functioning. Perhaps scramblers are making the best of a bad job.

Informational versus somatic state-based hypotheses

Nettle & Bateson (2015) recently provided conceptual clarity to explain the coexistence of alternative morphs by distinguishing between (i) informational hypotheses – like sexual selection theory – that state that input received during development provides information about the adult environment (like the mating arena), and (ii) somatic state-based hypotheses that state that the input received during development enduringly alters some aspect of the individual’s somatic state.

In case of a developmental plasticity like minors and majors, their expression is generally explained in an informational hypothesis by a dependence on an information cue (the developmental input) from the environment that informs on future (adult) phenotype performance (Oliveira et al. 2008). Neither fighters nor scramblers have a universally higher fitness because trade-offs exist, and the relative fitnesses of the alternative morphs are contingent upon the environmental conditions. If the information cue increases the probability that the morph produced has the highest fitness in the expected (future) environment, such induction of morph expression is adaptive (see below: Fig. 1A) (Nettle & Bateson 2015).

Somatic state-based hypotheses assume that environmental conditions can causally affect the somatic state of an individual, like its size or muscular strength, and thereby affect male morph expression. In the bulb mite R. robini (see below: Fig. 1B), the lower the food quality (the developmental input), the smaller the size, or somatic state, of adult males (Leigh & Smallegange 2014). Secondly, male morph expression can be independent of size in R. robini (Leigh & Smallegange 2014): a small individual could be a fighter and a large one a scrambler. What is then assumed to have evolved is a mechanism linking the two together (Nettle & Bateson 2015): the switching rule ‘if you find yourself large, become a fighter; if you find yourself small, become a scrambler’. For this rule to be adaptive, the optimal morph must be dependent on somatic state: expected fitness of a large male R. robini must be higher if it becomes a fighter than if it does not, while the opposite must be true for a small male R. robini (Nettle & Bateson 2015) (see below: Fig. 1C). Crucially, morph expression is not dependent on a cue from the environment that informs on future morph performance; instead, the decision to develop into which morph is based on the current somatic state of the individual.


Figure 1. After Nettle and Bateson (2015; Fig. 1). The two types of hypotheses that explain adaptive developmental plasticity are grouped as (A) informational hypotheses, where the developmental input provides information about the adult environment as a result of which an individual develops the morphology (grey block) like thickened legs of fighter mites (B) or not, and (C) somatic state-based hypotheses, where the developmental input enduringly alters some aspect of an individual’s somatic state and the individual develops the morphology (grey block) or not (Nettle & Bateson 2015).

So, what’s happening with these male mites?

There is some evidence to suggest that a resource allocation trade-off between fighter leg development and other somatic functions exists as (i) fighter leg development happens simultaneously with the final moult to the adult stage in a closed developmental system, and (ii) fighter males shrink during maturation, whereas scrambler males do not (Smallegange et al. 2012). However, we do not know whether males with small resource budgets are particularly negatively affected by this trade-off and therefore refrain from developing fighter legs. Flor Rhebergen (@FRhebergen) of the DynaMite lab, however, is focusing his PhD research on unravelling to what extent male morph coexistence in the bulb mite can be explained by a somatic state-based hypothesis. His findings will provide new insights into the maintenance of alternative morphs in single populations. I can’t way to see them!


Leigh DM, Smallegange IM. 2014. ​ Effects of variation in nutrition on male morph development in the bulb mite Rhizoglyphus robini. Journal of Experimental and Applied Acarology 64: 159-170

Nettle D, Bateson M. 2015. Adaptive developmental plasticity: what is it, how can we recognize it and when can it evolve? Proceedings of the Royal Society London Series B 282:20151005

Oliveira RF, Taborsky M, Brockmann HJ (Eds.), 2008. Alternative Reproductive Tactics. Cambridge University Press, Cambridge.

Radwan JW. 2009. Alternative mating tactics in acarid mites. Pp. 185–208 in Advances in the Study of Behavior, Vol. 39. Elsevier Academic Press, San Diego.

Smallegange IM, Charalambous M, Thorne N. 2012. Fitness trade-offs and the maintenance of alternative male morphs in the bulb mite (Rhizoglyphus robini). Journal of Evolutionary Biology 25:972-980.

Van den Beuken, TPG, Smallegange IM. 2018. Life history consequences of nutritional history in a male dimorphic mite: evidence for a nuptial gift? Evolutionary Ecology 32: 411-425

Van den Beuken TPG, Duinmeijer CC, Smallegange IM. 2019. Costs of weaponry: unarmed males sire more offspring than armed males in a male-dimorphic mite. Journal of Evolutionary Biology 32: 153-162

*A similar version of this post was posted on


Author biography: Isabel Smallegange is an Associate Professor of Population Biology at the University of Amsterdam.  Follow her @I_Smallegange, or check out her blogs at, where she also discusses issues regarding the work-life balance in academia.