Light environment influences mating behaviours during the early stages of divergence in tropical butterflies

Abstract

Speciation is facilitated when traits under divergent selection also act as mating cues. Fluctuations in sensory conditions can alter signal perception independently of adaptation to the broader sensory environment, but how this fine-scale variation may constrain or promote behavioural isolation has received little attention. The warning patterns of Heliconius butterflies are under selection for aposematism and act as mating cues. Using computer vision, we extracted behavioural data from 1481 h of video footage, for 387 individuals. We show that the putative hybrid species H. heurippa and its close relative H. timareta linaresi differ in their response to divergent warning patterns, but that these differences are strengthened with increased local illuminance. Trials with live individuals reveal low-level assortative mating that is sufficiently explained by differences in visual attraction. Finally, results from hybrid butterflies are consistent with linkage between a major warning pattern gene and the corresponding behaviour, though the differences in behaviour we observe are unlikely to cause rapid reproductive isolation as predicted under a model of hybrid trait speciation. Overall, our results reveal that the contribution of ecological mating cues to reproductive isolation may depend on the immediate sensory conditions during which they are displayed to conspecifics.

Does sexual conflict contribute to the evolution of novel warning patterns?

“…The results of our experiments with H. timareta may simply reflect the lack of strong differences in visual attraction. In particular, mate choice experiments with H. t. linaresi males – which were run concurrently with experiments reported here – revealed that males show only very weak preferences for the conspecific yellow pattern over a yellow-red pattern, as used in the present study (Hausmann et al 2021). Recently, it has also become apparent that the composite color patterns of H. heurippa may not be the target of differences in male attraction between different species of Heliconius (Mavárez et al 2021).…”

“…1B) were collected from Guayabal (2°41’04”N, 74°53’17”W) and H. heurippa (yellow and red forewing bar) from Lejanías (03°34’0”N, 74°04’20.4”W), Buenavista (4°10’30”N, 73°40’41”W) and Santa María (04°53’28.2”N, 73°15’11.4”W) in Colombia. Outbred stocks were established and used to generate H. t. linaresi x H. heurippa F1 and backcrosses to H. t. linaresi hybrids (as described in Hausmann et al 2021). The presence of the red forewing band is controlled by a single Mendelian locus ( optix ), and segregates in the backcross to H. t. linaresi so that equal numbers of individuals display a (‘novel’) yellow-red forewing band phenotype or a (‘control’) yellow forewing phenotype (Fig.…”

“…Since then, numerous experiments have repeatedly shown that male Heliconius generally prefer ‘females’ that share their own warning pattern over that of other conspecific morphs or closely related species (e.g. Jiggins et al 2001, 2004; Kronforst et al 2006; Merrill et al 2011b, 2011a, 2014, 2019; Sánchez et al 2015; Hausmann et al 2021). It seems likely that competition between males drives these genetically determined local preferences, as the ability to efficiently locate potential mates within a visually complex environment would be beneficial (Merrill et al 2019).…”

Does sexual conflict contribute to the evolution of novel warning patterns?

“…H. timareta linaresi (yellow forewing bar; Figure 1b) were collected from Guayabal (2°41′04″N, 74°53′17″W) and H. heurippa (yellow and red forewing bar) from Lejanías (03°34′0″N, 74°04′20.4″W), Buenavista (4°10′30″N, 73°40′41″W) and Santa María (04°53′28.2″N, 73°15′11.4″W) in Colombia. Outbred stocks were established and used to generate H. t. linaresi × H. heurippa F 1 and backcrosses to H. t. linaresi hybrids (as described in Hausmann et al, 2021). The presence of the red forewing band is controlled by a single Mendelian locus ( optix ), and segregates in the backcross to H. t. linaresi so that equal numbers of individuals display a (novel) yellow‐red forewing band phenotype or a (control) yellow forewing phenotype (Figure 1b).…”

Insect opsins and evo-devo: what have we learned in 25 years?

“…In other insects, relatively little is known about development and opsin regulation, despite Hymenoptera and Lepidoptera being major visual ecology models [52][53][54]. One key theme to emerge in the last 25 years is the understanding of homology between the inner colour photoreceptor cells between D. melanogaster, Lepidoptera, and Hymenoptera.…”