Mate Preference for a Phenotypically Plastic Trait Is Learned, and May Facilitate Preference-Phenotype Matching

Abstract

Fixed, genetically determined, mate preferences for species whose adult phenotype varies with rearing environment may be maladaptive, as the phenotype that is most fit in the parental environment may be absent in the offspring environment. Mate preference in species with polyphenisms (environmentally dependent alternative phenotypes) should therefore either not focus on polyphenic traits, be polyphenic themselves, or learned each generation. Here, we test these alternative hypotheses by first describing a female-limited seasonal polyphenism in a sexually dimorphic trait in the butterfly Bicyclus anynana, dorsal hindwing spot number (DHSN), and then testing whether male and female mate preferences for this trait exist, and whether they are seasonally polyphenic, or learned. Neither naïve males nor naïve females in either seasonal form exhibited mating preferences for DHSN. However, males, but not females, noticed DHSN variation and learned mate preferences for DHSN. These results suggest that individuals may accommodate environmentally dependent variation in morphological traits via learned mate preferences in each generation, and that learned mate preference plasticity can be sexually dimorphic. K E Y W O R D S :Bicyclus anynana, mate choice, seasonal polyphenism, sexual dimorphism, sexual imprinting.

Dense, small and male-biased cages exacerbate male–male competition and reduce female choosiness in Bicyclus anynana

“…Nevertheless, in our study when the OSR was biased towards females, sex role did not seem to be totally reversed as female choosiness appeared to increase with increasing densities: females escaped more often and more rapidly from male mating attempts with increasing density. Therefore, mutual mate choice appeared to vary with density under the female-biased sex ratio in our study, suggesting that mutual mate choice in B. anynana occurs in the wet seasonal form and not only at the level of the seasonal sex role reversal of the species (Prudic et al, 2011;Westerman, Chirathivat, et al, 2014).…”

“…OSR, Arnqvist, 1992;Kokko et al, 2012;Krupa & Sih, 1993;density, Jirotkul, 1999b;Mills & Reynolds, 2003;Pomfret & Knell, 2008;Rowe et al, 1994). In B. anynana, there has long been a general agreement that female choice should prevail in the wet seasonal form (van Bergen et al, 2013;Brakefield et al, 2001;Costanzo & Monteiro, 2007;Frankino, Zwaan, Stern, & Brakefield, 2007;Nieberding et al, 2008Nieberding et al, , 2012Prudic et al, 2011;Robertson & Monteiro, 2005;Westerman, Chirathivat, Schyling, & Monteiro, 2014;Westerman, Drucker, & Monteiro, 2014;Westerman, HodginsDavis, Dinwiddie, & Monteiro, 2012;Westerman & Monteiro, 2013). This is notably based on the facts that females do reject courting males, rarely mate more than once in the field and in the laboratory (van Bergen et al, 2013;Brakefield et al, 2001;Brakefield & Reitsma, 1991;Joron & Brakefield, 2003;Nieberding et al, 2008Nieberding et al, , 2012, and gain neither direct benefits (no evidence for nuptial gifts, Ferkau & Fischer, 2006;M€ olleman, Zwaan, & Brakefield, 2004; but see Prudic et al, 2011;Westerman, Drucker, et al, 2014, who suggest that females may receive a beneficial nuptial gift from dry season males) nor fitness benefits from multiple matings while suffering survival costs (Fischer, 2007).…”

Colour polymorphism torn apart by opposing positive frequency‐dependent selection, yet maintained in space

“…Specifically, male B. anynana have been shown to learn preferences to mate with particular phenotypes of females with dorsal hind wing eyespot numbers, depending on pre‐mating experience with that phenotype (Westerman et al . ). It is suggested that in this system plastic mate preferences, rather than pre‐existing mating biases, allow male B. anynana butterflies the opportunity to choose the best mate in a highly fluctuating environment season, with social experiences providing the basis for learning.…”

Transgenerational inheritance of learned preferences for novel host plant odors inBicyclus anynanabutterflies

“…Bicyclus anynana is also a species where adults have previously been shown to learn a variety of different wing patterns (Westerman et al. , ; Westerman and Monteiro ) as well as pheromone odors (Dion et al. ).…”