Pervasive genetic associations between traits causing reproductive isolation in Heliconius butterflies

Ecological speciation proceeds through the accumulation of divergent traits that contribute to reproductive isolation, but in the face of gene flow traits that characterize incipient species may become disassociated through recombination. Heliconius butterflies are well known for bright mimetic warning patterns that are also used in mate recognition and cause both pre- and post-mating isolation between divergent taxa. Sympatric sister taxa representing the final stages of speciation, such as Heliconius cydno and Heliconius melpomene, also differ in ecology and hybrid fertility. We examine mate preference and sterility among offspring of crosses between these species and demonstrate the clustering of Mendelian colour pattern loci and behavioural loci that contribute to reproductive isolation. In particular, male preference for red patterns is associated with the locus responsible for the red forewing band. Two further colour pattern loci are associated, respectively, with female mating outcome and hybrid sterility. This genetic architecture in which ‘speciation genes’ are clustered in the genome can facilitate two controversial models of speciation, namely divergence in the face of gene flow and hybrid speciation.     

Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing

Heliconius butterflies represent a recent radiation of species, in which wing pattern divergence has been implicated in speciation. Several loci that control wing pattern phenotypes have been mapped and two were identified through sequencing. These same gene regions play a role in adaptation across the whole Heliconius radiation. Previous studies of population genetic patterns at these regions have sequenced small amplicons. Here, we use targeted next-generation sequence capture to survey patterns of divergence across these entire regions in divergent geographical races and species of Heliconius. This technique was successful both within and between species for obtaining high coverage of almost all coding regions and sufficient coverage of non-coding regions to perform population genetic analyses. We find major peaks of elevated population differentiation between races across hybrid zones, which indicate regions under strong divergent selection. These 'islands' of divergence appear to be more extensive between closely related species, but there is less clear evidence for such islands between more distantly related species at two further points along the 'speciation continuum'. We also sequence fosmid clones across these regions in different Heliconius melpomene races. We find no major structural rearrangements but many relatively large (greater than 1 kb) insertion/deletion events (including gain/loss of transposable elements) that are variable between races.     

Evolution of sexual size monomorphism: the influence of passive mate guarding

Some species have potential for intense mate competition yet exhibit little or no sexual size dimorphism, despite predictions from sexual selection theory. Using a conceptual model, we show the conditions for which passive mate guarding with copulatory plugs can be an alternative and more successful strategy to active (direct) guarding, reducing selection pressure on large male size. The model predicts that copulatory plugs in mammals should be favoured in species for which females have short sexual receptivity periods. Using data on 62 primate species and a phylogenetic regression approach, we show that, as predicted, copulatory plugs are negatively associated with degree of sexual dimorphism and females’ sexual receptivity length. Penile spines are also significantly associated with plug use and short receptivity periods suggesting a possible offensive role in sperm competition. Results highlight that life‐history characteristics, such as sexual receptivity lengths, may alter the costs and benefits of alternative male strategies and thus alter the strength of sexual selection.     

Parallel divergence in mate guarding behaviour following colonization of a novel habitat

Ecological factors can have profound effects on mating system and mating behaviour. We investigated the effect of altered ecological conditions, following colonization of a novel habitat, on precopulatory mate guarding in a freshwater isopod (Asellus aquaticus). This isopod occurs in two different ecotypes, which coexist within several different lakes in Sweden but which utilize different habitats. These ecotypes have rapidly (ca. 40 generations) diverged in parallel among lakes in several phenotypic characters, presumably as a response to different predatory pressures. Here, we demonstrate that also mate guarding characteristics have diverged in parallel between the ecotypes in different lakes. This is one of the few studies reporting parallel evolution of mating behaviour. Furthermore, our results also indicate a potential sexual conflict, as the length of mate guarding appears to lower components of female fitness. We discuss how novel environments might have strong and rapid effects on mate guarding dynamics and mating behaviour.     

Precopulatory mate guarding in Harpacticella inopinata Sars (Copepoda: Harpacticoida) from Lake Baikal

Precopulatory mate guarding is reported for the first time from a freshwater harpacticoid, Harpacticella inopinata. Adult males were observed grasping onto juvenile females from the third copepodid stage onwards, but most commonly with the fifth copepodid. This behaviour is interpreted as a plesiomorphic trait of the family Harpacticidae.     

Female butterflies prefer males bearing bright iridescent ornamentation

Butterflies are among nature's most colorful animals, and provide a living showcase for how extremely bright, chromatic and iridescent coloration can be generated by complex optical mechanisms. The gross characteristics of male butterfly colour patterns are understood to function for species and/or sex recognition, but it is not known whether female mate choice promotes visual exaggeration of this coloration. Here I show that females of the sexually dichromatic species Hypolimnas bolina prefer conspecific males that possess bright iridescent blue/ultraviolet dorsal ornamentation. In separate field and enclosure experiments, using both dramatic and graded wing colour manipulations, I demonstrate that a moderate qualitative reduction in signal brightness and chromaticity has the same consequences as removing the signal entirely. These findings validate a long-held hypothesis, and argue for the importance of intra- versus interspecific selection as the driving force behind the exaggeration of bright, iridescent butterfly colour patterns.     

The adaptive significance of mate guarding in the soapberry bug,Jadera Haematoloma (Hemiptera: Rhopalidae)

Male soapberry bugs (Jadera haematoloma)face severe mating competition at the northern edge of their range due to male-biased adult sex ratios. Copulations lasting up to 11 days may serve a mate guarding function (encompassing four or more ovipositions), but copulation duration is highly variable, with some pairings lasting as little as 10 min. Data were gathered to describe factors that influence the reproductive costs and benefits of prolonged copulation. Estimated copulation durations (mean ± SD) were 20 ± 23 h in the lab and 50 ± 8 h in the field and were only weakly affected by sex ratio. Females mated for 5 min produced as many fertile eggs as those mated for 600 min laid; they became depleted of fertile sperm after about 25 days. In twicemated females, the first male's paternity was reduced by about 60%, and all females (N = 13) whose mates were removed experimentally mated again within an average of 6 min. The outcome of sperm competition on a perclutch basis was not highly predictable. The possibility of increased sperm displacement in longer copulations was not tested. Males often guarded females during oviposition and successfully defended them from intruding single males by recopulating. Such intrusions occurred in the majority of oviposition attempts observed in nature. Even though most females mated promiscuously, in a focal aggregation with a mean sex ratio of 2.2 ± 0.4 males/female, the interval between matings by males was commonly several days. Males appeared to respond facultatively to several aspects of the distribution and availability of females. The intensities of mating competition and sperm competition indicate that monogamous mate guarding should be favored over nonguarding in nature. Unpredicted brief. pairings may result from assessment by males of female reproductive value or of their own physical condition, or from female resistance.     

Experimental evolution of a sexually selected display in yeast

The fundamental principle underlying sexual selection theory is that an allele conferring an advantage in the competition for mates will spread through a population. Remarkably, this has never been demonstrated empirically. We have developed an experimental system using yeast for testing genetic models of sexual selection. Yeast signal to potential partners by producing an attractive pheromone; stronger signallers are preferred as mates. We tested the effect of high and low levels of sexual selection on the evolution of a gene determining the strength of this signal. Under high sexual selection, an allele encoding a stronger signal was able to invade a population of weak signallers, and we observed a corresponding increase in the amount of pheromone produced. By contrast, the strong signalling allele failed to invade under low sexual selection. Our results demonstrate, for the first time, the spread of a sexually selected allele through a population, confirming the central assumption of sexual selection theory. Our yeast system is a powerful tool for investigating the genetics of sexual selection.     

The function of mate guarding in a field cricket (Orthoptera: Gryllidae;Teleogryllus natalensis otte and cade)

Three hypotheses relating to the function of postcopulatory mate guarding were tested for the cricketTeleogryllus natalensis. The hypothesis that guarding allows the male to remain with the female for repeated matings was rejected. This was because the mean intercopulatory interval for maleT. natalensis was found to be nearly twice as long as the mean duration of guarding. Nor do the results provide evidence to support the hypothesis that guarding functions to prevent copulation attempts by rival males (the rival exclusion hypothesis): the presence of a rival male was found to have no significant effect on the duration of spermatophore attachment for either guarded or unguarded females. The results do, however, support a third hypothesis, namely, that guarding functions to prevent the female from removing the spermatophore ampulla before complete sperm transfer. As predicted by this hypothesis, the presence of a guarding male was found to have a significant positive effect on the duration of spermatophore attachment. Further support for this hypothesis was provided by the fact that there was a significant positive correlation between the duration of mate guarding and the duration of spermatophore attachment.