Does male preference play a role in maintaining female limited polymorphism in a Batesian mimetic butterfly?

Abstract

Female-limited polymorphism occurs in multiple butterfly species with Batesian mimicry. While frequency-dependent selection is often argued as the driving force behind polymorphism in Batesian mimicry systems, male preference and alternative female mating strategies may also influence the maintenance of multiple female forms. Through a series of behavioural assays with the female-limited Batesian mimetic butterfly Papilio polytes, we show that males prefer stationary mimetic females over stationary non-mimetic females, but weigh female activity levels more heavily than female wing pattern when choosing between active mimetic and active non-mimetic females. Male preference for mimetic vs. non-mimetic females is independent of male genotype at the locus responsible for the female wing pattern, the autosomal gene doublesex. However male genotype does influence their response to active females. Male emphasis on female behaviour instead of appearance may reduce sexual selection pressures on female morphology, thereby facilitating frequency-dependent natural selection due to predation risk and toxic model abundance.

Behaviour before beauty: Signal weighting during mate selection in the butterfly Papilio polytes

“…Male P. polytes prefer mimetic wing patterns when choosing between two inactive females in the presence of other males, but prefer active females independent of female wing pattern when choosing between two females allowed to move and in the absence of other males (Westerman et al, 2018). Male P. polytes prefer mimetic wing patterns when choosing between two inactive females in the presence of other males, but prefer active females independent of female wing pattern when choosing between two females allowed to move and in the absence of other males (Westerman et al, 2018).…”

“…Butterfly species, many of which are polymorphic, have been found to use a number of different signals during the mate selection process (Costanzo & Monteiro, 2007;Papke, Kemp, & Rutowski, 2007;Westerman et al, 2018;Wiklund & Kaitala, 1995). Some of these signals may be redundant, while others may convey unique information.…”

“…For example, females use pheromone concentration to assess male age (Nieberding et al, 2012); males use female size to assess female reproductive potential (Wedell & Cook, 1999); and both sexes are known to attend to the wing patterns of the opposite sex, though the specific information conveyed through these wing patterns is often unclear (Chamberlain, Hill, Kapan, Gilbert, & Kronforst, 2009;Chouteau, Llaurens, Piron-Prunier, & Joron, 2017;Melo, Salazar, Jiggins, & Linares, 2009;Morehouse & Rutowski, 2010;Obara, Koshitaka, & Arikawa, 2008;Robertson & Monteiro, 2005) (but see . Activity levels may also be used by both sexes in the mate selection process, and are hypothesized to convey information related to current condition (Westerman, Drucker, & Monteiro, 2014;Westerman et al, 2018). Activity levels may also be used by both sexes in the mate selection process, and are hypothesized to convey information related to current condition (Westerman, Drucker, & Monteiro, 2014;Westerman et al, 2018).…”

“…Batesian mimics such as Papilio polytes, Papilio glaucus and Papilio dardanus, on the other hand, have served as models for the study of female-limited polymorphism (Cook, Vernon, Bateson, & Guilford, 1994;Kunte, 2009;Kunte et al, 2014;Nishikawa et al, 2015). The non-mimetic female form is ancestral (Zhang, Westerman, Nitzany, Palmer, & Kronforst, 2017), and the maintenance of this non-mimetic female form in populations containing mimetic females is hypothesized to be due to frequency-dependent predation pressure, male preference for the non-mimetic form and/or increased fecundity resulting from reduced male harassment (reviewed in Kunte, 2009;Westerman et al, 2018). The non-mimetic female form is ancestral (Zhang, Westerman, Nitzany, Palmer, & Kronforst, 2017), and the maintenance of this non-mimetic female form in populations containing mimetic females is hypothesized to be due to frequency-dependent predation pressure, male preference for the non-mimetic form and/or increased fecundity resulting from reduced male harassment (reviewed in Kunte, 2009;Westerman et al, 2018).…”

“…In many of these Batesian mimetic systems, one or many female forms mimic the wing patterns of distantly related toxic butterflies, while an additional female form is non-mimetic and male-like. Male P. glaucus have been found to prefer the non-mimetic female form (Burns, 1966;Levin, 1973), while male P. polytes use at least two signals when determining whom to court: female wing pattern and female activity levels (Westerman et al, 2018), suggesting that male preference may play a role in the maintenance of femalelimited polymorphism in both of these Batesian mimetic species. Male P. glaucus have been found to prefer the non-mimetic female form (Burns, 1966;Levin, 1973), while male P. polytes use at least two signals when determining whom to court: female wing pattern and female activity levels (Westerman et al, 2018), suggesting that male preference may play a role in the maintenance of femalelimited polymorphism in both of these Batesian mimetic species.…”