The fitness effects of a pale mutant in the aposematic seed bugLygaeus simulansindicate pleiotropy between warning coloration and life history

Abstract

Conspicuous warning colors that signal chemical or other defenses are common in the natural world. For instance, such aposematic warning patterns of red‐and‐black or yellow‐and‐black are common among insect taxa, particularly in the order Hemiptera, often forming the basis of Batesian and/or Müllerian mimicry rings. In addition, it has been repeatedly noted that color polymorphisms or mutants that influence pigmentation can show pleiotropy with other behavioral, physiological, or life‐history traits. Here, we describe a pale mutant of the seed bug Lygaeus simulans that appeared in our laboratory population in 2012, which differs in color to the wild‐type bugs. Through multigenerational experimental crosses between wild‐type and pale mutant L. simulans, we first show that the pale phenotype segregates as a single Mendelian locus, with the pale allele being recessive to the wild type. Next, we show (a) that there is a large heterozygous advantage in terms of fecundity, (b) that pale females suffer reduced longevity, and (c) that pale males have increased body length compared to wild‐type homozygotes. Our data therefore suggest that the color locus is pleiotropic with a number of life‐history traits, opening the door for a more complete genetic analysis of aposematic coloration in this species. In addition, this phenotype will be useful as a visible genetic marker, providing a tool for investigating sperm competition and other post‐copulatory drivers of sexual selection in this species.

Mating failure shapes the patterns of sperm precedence in an insect

“…This confirms previous findings (Dougherty and Shuker 2014). Larger females are more fecund (Balfour et al 2018), so males will likely gain more fitness benefits from mating with large than small females. Males also appeared to be more willing to engage in copulation with once-mated than virgin females, as has previously been found in this and the sister species L. equestris (Sillén-Tullberg 1981;Micholitsch et al 2000).…”

“…Finally, we excluded 18 data points from the analysis because of the 'wrong' morph of nymphs appearing in the F1 or nymphs being present when the pairs were not observed to mate for > 30 min (the putative minimum time needed for sperm transfer). Reasons to explain these data anomalies include heterozygous males being present in small numbers in the wild-type population cages and eggs being accidentally transferred via forceps from one box to another (see also Balfour et al 2018 for discussion, including evidence for the pale morph segregating at very low frequency in wild-type lab populations) or, indeed, sperm being transferred by males in copulations < 30 min in duration. Therefore, the final sample sizes were N = 229, 241, 160 and 161 for treatments PPW, PWP, PPP and PWW, respectively.…”

“…Since then, a minimum of two population cages of pale L. simulans have been maintained in the lab (Balfour et al 2018). The locus for colour morph in L. simulans is inherited in a Mendelian fashion, with a dominant wild-type allele resulting in the typical red and black aposematic colouration and a recessive pale mutant allele resulting in paler green-brown coloured bugs (Balfour et al 2018). Here, we used this colour morph as a phenotypic marker to carry out the following experiment and assign paternity to the offspring sired.…”

“…Dougherty and Shuker 2014;Greenway et al 2017). These bugs make an excellent study species for investigating the effects of mating failure on paternity outcome, not only because they are easy to rear in the lab, mate multiply and express these high levels of mating failure (Burdfield-Steel and Shuker 2014; Greenway et al 2017) but also because we can now use a genetically-based colour polymorphism as a morphological marker to estimate paternity (Balfour et al 2018). Importantly, mating failure in this species has been found to be almost exclusively due to insemination failure: dissections showed that 92.6% of females that exhibited mating failure had received no sperm during copulation .…”

A single pleiotropic locus influences the rate of hybridization between two sibling species of Lygaeus bugs

“…We have previously shown that female L. equestris can mate and hybridize with male L. simulans , but not the other way around, an example of the asymmetric reproductive isolation described above (Evans et al., 2015). We have also recently isolated and described a pale mutant color morph of L. simulans (Balfour et al., 2018). Although no evidence for this pale mutant exists in the wild, a potentially similar “gray” mutant was recorded in the laboratory by Sillén‐Tullberg (1985) in L. equestris .…”