Evidence for a third male type in a male‐dimorphic model species

Stewart, Kathryn A.; Beuken, Tom P. G. Van den; Rhebergen, Flor T.; Deere, Jacques A.; Smallegange, Isabel M.

doi:10.1002/ecy.2239

Cited by 12 publications

(15 citation statements)

References 15 publications

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“…It should be emphasized however, that this study does not provide evidence that all scramblers are female mimics, as the model that best describes the data did not differentiate between male ARTs. Nevertheless, the results of this study do warrant further exploration of a female mimic or "sneaking" strategy in bulb mites, particularly because 'megascramblers'-which sometimes elicit mating behavior from other males-are suggested to be a third ART [47]. Indeed, these mega-scramblers may be the result of sexual selection driving larger scramblers to chemically and physically resemble females.…”

Section: Intersexual and Intrasexual Differences In Pheromone Productionmentioning

confidence: 77%

“…Importantly, ART expression in R. robini does not depend on population density, unlike in its sister species R. echinopus [41], nor on ART frequency [42]. Upon maturity, male R. robini develop into one of two distinct morphs (see Figure 1): (1) juvenile males that are relatively large mostly mature as "fighters", which possess a thickened third leg pair with a sharp end that can be used to kill conspecifics [45,46], and (2) juvenile males that are relatively small mostly mature as "scramblers", which lack the weaponized leg pair (although a rare third morph, the megascrambler, has recently been suggested; [47]). Although scrambler expression is regulated by a (partially) genetically determined threshold for body size [17; 48; 49], gene-by-environment interactions also play a key role [50], with diet quality and quantity thought to be the primary drivers of body size and therefore ART expression [18].…”

Section: Introductionmentioning

confidence: 99%

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Toward an understanding of the chemical ecology of alternative reproductive tactics in the bulb mite (Rhizoglyphus robini)

Zeeman

Smallegange

Steel

et al. 2021

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Background Under strong sexual selection, certain species evolve distinct intrasexual, alternative reproductive tactics (ARTs). In many cases, ARTs can be viewed as environmentally cued threshold traits, such that ARTs coexist if their relative fitness alternates over the environmental cue gradient. Surprisingly, the chemical ecology of ARTs has been underexplored in this context. To our knowledge, no prior study has directly quantified pheromone production for ARTs in a male polymorphic species. Here, we used the bulb mite — in which males are either armed fighters that kill conspecifics, or unarmed scramblers — as a model system to gain insight into the role of pheromones in the evolutionary maintenance of ARTs. Given that scramblers forgo investment into weaponry, we tested whether scramblers produce higher pheromone quantities than fighters, which would improve the fitness of the scrambler phenotype, e.g. through female mimicry to avoid aggression from competitors. To this end, we sampled mites from a rich and a poor nutritional environment and quantified their production of the female sex pheromone α acaridial through gas chromatography analysis. Results We found a positive relationship between pheromone production and body size, but males exhibited a steeper slope in pheromone production with increasing size than females. Females exhibited a higher average pheromone production than males. We found no significant difference in slope of pheromone production over body size between fighters and scramblers. However, scramblers reached larger body sizes and higher pheromone production than fighters, providing some evidence for a potential female mimic strategy adopted by large scramblers. Pheromone production was significantly higher in mites from the rich nutritional environment than the poor environment. Conclusion Further elucidation of pheromone functionality in bulb mites, and additional inter and intrasexual comparisons of pheromone profiles are needed to determine if the observed intersexual and intrasexual differences in pheromone production are adaptive, if they are a byproduct of allometric scaling, or diet mediated pheromone production under weak selection. We argue chemical ecology offers a novel perspective for research on ARTs and other complex life-history traits.

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Section: Intersexual and Intrasexual Differences In Pheromone Productionmentioning

confidence: 77%

Section: Introductionmentioning

confidence: 99%

Toward an understanding of the chemical ecology of alternative reproductive tactics in the bulb mite (Rhizoglyphus robini)

Zeeman

Smallegange

Steel

et al. 2021

Preprint

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“…Recently, a third male morph termed the mega-scrambler has been identified in R. robini (Stewart, van den Beuken, Rhebergen, Deere, & Smallegange, 2018). Systems comprising three ARTs are not uncommon (Rowland & Emlen, 2009;Shuster & Sassaman, 1997;Sinervo & Lively, 1996), which raises the question of how the model could be extended to address three-ART systems.…”

Section: Discussionmentioning

confidence: 99%

An eco‐evolutionary feedback loop between population dynamics and fighter expression affects the evolution of alternative reproductive tactics

Croll

Egas

Smallegange

2018

Journal of Animal Ecology

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Surprisingly, little is known about how eco-evolutionary feedback loops affect trait dynamics within a single population. Polymorphisms of discrete alternative phenotypes present ideal test beds to investigate this, as the alternative phenotypes typically exhibit contrasting demographic rates mediated through frequency or density dependence, and are thus differentially affected by selection. Alternative reproductive tactics (ARTs), like male fighters and sneakers, are an extreme form of discrete phenotype expression and occur across many taxa. Fighters possess weapons for male-male competition over access to mates, whereas sneakers are defenceless but adopt tactics like female-mimicking. Because fighters in some species mortally injure conspecifics, this raises the question whether fighter expression can feed back to affect population size and structure, thereby altering the selection gradient and evolutionary dynamics of ART expression in an eco-evolutionary feedback loop. Here, we investigated how the eco-evolutionary feedback loop between fighter expression and population size and structure affects the evolution and maintenance of ARTs. We introduced intraspecific killing by fighters in a two-sex, two-ART population model parameterized for the male dimorphic bulb mite (Rhizoglyphus robini) that includes life-history differences between the ARTs and a mating-probability matrix analogous to the classic hawk-dove game. Using adaptive dynamics, we found that the intraspecific killing by fighters can extend the range of life-history parameter values under which ARTs evolve, because fighters that kill other fighters decrease fighter fitness. This effect can be nullified when benefits from killing are incorporated, like increased reproduction through increased energy uptake. The eco-evolutionary feedback effects found here for a dimorphic trait likely also occur in other fitness-related traits, such as behavioural syndromes, parental care and niche construction traits. Current theoretical advances to model eco-evolutionary processes, and empirical steps towards unravelling the underlying drivers, pave the way for understanding how selection affects trait evolution in an eco-evolutionary feedback loop.

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“…Although it is well established that the alternative morphs in R. robini are associated with variation in body size, and thus represent a discontinuous allometric scaling relationship (Smallegange, 2011; Leigh & Smallegange, 2014; Smallegange & Deere, 2014), the correlation is noisy. A large range of overlap in body size exists between juveniles developing as fighters and juveniles developing as scramblers (Smallegange, 2011; Stewart et al ., 2018). We hypothesize that these observations are, at least partly, explained by food-dependent plasticity in how body size scales with male morph expression.…”

Section: Introductionmentioning

confidence: 99%

Nutrient-dependent allometric plasticity in a male-diphenic mite

Rhebergen

2021

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Male secondary sexual traits often scale allometrically with body size. These allometries can be variable within species, and may shift depending on environmental conditions such as food quality. Such allometric plasticity has been hypothesized to initiate local adaptation and evolutionary diversification of scaling relationships, but is under-recorded, and its eco-evolutionary effects are not well understood. Here, we test for allometric plasticity in the bulb mite (Rhizoglyphus robini) in which large males tend to develop as armed adult fighters with thickened third legs, while small males become adult scramblers without thickened legs. We first examined the ontogenetic timing for size- and growth-dependent male morph determination, using experimentally amplified fluctuations in growth rate throughout juvenile development. Having established that somatic growth and body size determine male morph expression immediately before metamorphosis, we examined whether the relationship between adult male morph and size at metamorphosis shifts with food quality. We found that the threshold body size for male morph expression shifts towards lower values with deteriorating food quality, confirming food-dependent allometric plasticity. Such allometric plasticity may allow populations to track prevailing nutritional conditions, potentially facilitating rapid evolution of allometric scaling relationships.

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Evidence for a third male type in a male‐dimorphic model species

Cited by 12 publications

References 15 publications

Toward an understanding of the chemical ecology of alternative reproductive tactics in the bulb mite (Rhizoglyphus robini)

Toward an understanding of the chemical ecology of alternative reproductive tactics in the bulb mite (Rhizoglyphus robini)

An eco‐evolutionary feedback loop between population dynamics and fighter expression affects the evolution of alternative reproductive tactics

Nutrient-dependent allometric plasticity in a male-diphenic mite

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