skip to main content

Title: The effects of heterospecific mating frequency on the strength of cryptic reproductive barriers

Heterospecific mating frequency is critical to hybrid zone dynamics and can directly impact the strength of reproductive barriers and patterns of introgression. The effectiveness of post‐mating prezygotic (PMPZ) reproductive barriers, which include reduced fecundity via heterospecific matings and conspecific sperm precedence, may depend on the number, identity and order of mates. Studies ofPMPZbarriers suggest that they may be important in many systems, but whether these barriers are effective at realistic heterospecific mating frequencies has not been tested. Here, we evaluate the strength of cryptic reproductive isolation in two leaf beetles (Chrysochus auratusandC. cobaltinus) in the context of a range of heterospecific mating frequencies observed in natural populations. We found both species benefited from multiple matings, but the benefits were greater inC. cobaltinusand extended to heterospecific matings. We found thatPMPZbarriers greatly limited hybrid production byC. auratusfemales with moderate heterospecific mating frequencies, but that their effectiveness diminished at higher heterospecific mating frequencies. In contrast, there was no evidence forPMPZbarriers inC. cobaltinusfemales at any heterospecific mating frequency. We show that integrating realistic estimates of cryptic isolation with information on relative abundance and heterospecific mating frequency in the field substantially improves our understanding of the strong directional bias in F1 production previously documented in theChrysochushybrid zone. Our results demonstrate that heterospecific mating frequency is critical to understanding the impact of cryptic post‐copulatory barriers on hybrid zone structure and dynamics, and that future studies of such barriers should incorporate field‐relevant heterospecific mating frequencies.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Journal of Evolutionary Biology
Medium: X Size: p. 900-912
["p. 900-912"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    FemaleDrosophila melanogasterfrequently mate with multiple males in nature as shown through parentage analysis. Although polyandry is well documented, we know little about the timing between mating events in wild Drosophila populations due to the challenge of following behaviours of individual females. In this study, we used the presence of a male reproductive protein that is transferred to the female during mating (Sex Peptide,SP) to determine whether she had recently mated. We sampled females throughout the day, conducted control matings to determine the decay rate ofSPwithin the female reproductive tract and performed computer simulations to fit the observed proportion of mated females to a nonhomogenous Poisson process that defined the expected time between successive matings for a given female. In our control matings, 100% of mated females tested positive forSP0.5 h after the start of mating (ASM), but only 24% tested positive 24 hASM. Overall, 35% of wild‐caught females tested positive for the presence ofSP. Fitting our observed data to our simple nonhomogenous Poisson model provided the inference that females are mating, on average, approximately every 27 h (with 95% credibility interval 23–31 h). Thus, it appears that females are mating a bit less frequently that once per day in this natural population and that mating events tend to occur either early in the morning or late in the afternoon.

    more » « less
  2. Abstract

    Steep genetic clines resulting from recent secondary contact between previously isolated taxa can either gradually erode over time or be stabilized by factors such as ecological selection or selection against hybrids. We used patterns of variation in 30 nuclear and two mitochondrialSNPs to examine the factors that could be involved in stabilizing clines across a hybrid zone between two subspecies of the Atlantic killifish,Fundulus heteroclitus. Increased heterozygote deficit and cytonuclear disequilibrium in populations near the center of the mtDNAcline suggest that some form of reproductive isolation such as assortative mating or selection against hybrids may be acting in this hybrid zone. However, only a small number of loci exhibited these signatures, suggesting locus‐specific, rather than genomewide, factors. Fourteen of the 32 loci surveyed had cline widths inconsistent with neutral expectations, with twoSNPs in the mitochondrial genome exhibiting the steepest clines. Seven of the 12 putatively non‐neutral nuclear clines were forSNPs in genes related to oxidative metabolism. Among these putatively non‐neutral nuclear clines,SNPs in two nuclear‐encoded mitochondrial genes (SLC25A3 andHDDC2), as well asSNPs in the myoglobin, 40S ribosomal protein S17, and actin‐bindingLIMprotein genes, had clines that were coincident and concordant with the mitochondrial clines. When hybrid index was calculated using this subset of loci, the frequency distribution of hybrid indices for a population located at the mtDNAcline center was non‐unimodal, suggesting selection against advanced‐generation hybrids, possibly due to effects on processes involved in oxidative metabolism.

    more » « less
  3. Abstract

    We present a phylogeographic study of at least six reproductively isolated lineages of new world harvester ants within thePogonomyrmex barbatusandP. rugosusspecies group. The genetic and geographic relationships within this clade are complex: Four of the identified lineages show genetic caste determination (GCD) and are divided into two pairs. Each pair has evolved under a mutualistic system that necessitates sympatry. These paired lineages are dependent upon one another because theirGCDrequires interlineage matings for the production of F1 hybrid workers, and intralineage matings are required to produce queens. ThisGCDsystem maintains genetic isolation among these interdependent lineages, while simultaneously requiring co‐expansion and emigration as their distributions have changed over time. It has also been demonstrated that three of these fourGCDlineages have undergone historical hybridization, but the narrower sampling range of previous studies has left questions on the hybrid parentage, breadth, and age of these groups. Thus, reconstructing the phylogenetic and geographic history of this group allows us to evaluate past insights and hypotheses and to plan future inquiries in a more complete historical biogeographic context. Using mitochondrialDNAsequences sampled across most of the morphospecies’ ranges in the U.S.A. and Mexico, we conducted a detailed phylogeographic study. Remarkably, our results indicate that one of theGCDlineage pairs has experienced a dramatic range expansion, despite the genetic load and fitness costs of theGCDsystem. Our analyses also reveal a complex pattern of vicariance and dispersal inPogonomyrmexharvester ants that is largely concordant with models of late Miocene, Pliocene, and Pleistocene range shifts among various arid‐adapted taxa in North America.

    more » « less
  4. Abstract

    The genetic architecture of local adaptation has been of central interest to evolutionary biologists since the modern synthesis. In addition to classic theory on the effect size of adaptive mutations by Fisher, Kimura and Orr, recent theory addresses the genetic architecture of local adaptation in the face of ongoing gene flow. This theory predicts that with substantial gene flow between populations local adaptation should proceed primarily through mutations of large effect or tightly linked clusters of smaller effect loci. In this study, we investigate the genetic architecture of divergence in flowering time, mating system‐related traits, and leaf shape betweenMimulus laciniatusand a sympatric population of its close relativeM. guttatus. These three traits are probably involved inM. laciniatus’adaptation to a dry, exposed granite outcrop environment. Flowering time and mating system differences are also reproductive isolating barriers making them ‘magic traits’. Phenotypic hybrids in this population provide evidence of recent gene flow. Using next‐generation sequencing, we generate denseSNPmarkers across the genome and map quantitative trait loci (QTLs) involved in flowering time, flower size and leaf shape. We find that interspecific divergence in all three traits is due to fewQTLof large effect including a highly pleiotropicQTLon chromosome 8. ThisQTLregion contains the pleiotropic candidate gene TCP4 and is involved in ecologically important phenotypes in otherMimulusspecies. Our results are consistent with theory, indicating that local adaptation and reproductive isolation with gene flow should be due to few loci with large and pleiotropic effects.

    more » « less
  5. Mating cues evolve rapidly and can contribute to species formation and maintenance. However, little is known about how sexual signals diverge and how this variation integrates with other barrier loci to shape the genomic landscape of reproductive isolation. Here, we elucidate the genetic basis of ultraviolet (UV) iridescence, a courtship signal that differentiates the males of Colias eurytheme butterflies from a sister species, allowing females to avoid costly heterospecific matings. Anthropogenic range expansion of the two incipient species established a large zone of secondary contact across the eastern United States with strong signatures of genomic admixtures spanning all autosomes. In contrast, Z chromosomes are highly differentiated between the two species, supporting a disproportionate role of sex chromosomes in speciation known as the large-X (or large-Z) effect. Within this chromosome-wide reproductive barrier, linkage mapping indicates that cis- regulatory variation of bric a brac ( bab ) underlies the male UV-iridescence polymorphism between the two species. Bab is expressed in all non-UV scales, and butterflies of either species or sex acquire widespread ectopic iridescence following its CRISPR knockout, demonstrating that Bab functions as a suppressor of UV-scale differentiation that potentiates mating cue divergence. These results highlight how a genetic switch can regulate a premating signal and integrate with other reproductive barriers during intermediate phases of speciation. 
    more » « less