How barriers to gene flow arise and are maintained are key questions in evolutionary biology. Speciation research has mainly focused on barriers that occur either before mating or after zygote formation. In comparison, postmating prezygotic (PMPZ) isolation-a barrier that acts after gamete release but before zygote formation-is less frequently investigated but may hold a unique role in generating biodiversity. Here we discuss the distinctive features of PMPZ isolation, including the primary drivers and molecular mechanisms underpinning PMPZ isolation. We then present the first comprehensive survey of PMPZ isolation research, revealing that it is a widespread form of prezygotic isolation across eukaryotes. The survey also exposes obstacles in studying PMPZ isolation, in part attributable to the challenges involved in directly measuring PMPZ isolation and uncovering its causal mechanisms. Finally, we identify outstanding knowledge gaps and provide recommendations for improving future research on PMPZ isolation. This will allow us to better understand the nature of this often-neglected reproductive barrier and its contribution to speciation.

• MeSH
• Reproductive Isolation * MeSH
• Gene Flow MeSH
• Genetic Speciation * MeSH
• Animals MeSH
• Zygote * metabolism   MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Review MeSH

BACKGROUND: The common bedbug Cimex lectularius is a widespread ectoparasite on humans and bats. Two genetically isolated lineages, parasitizing either human (HL) or bat (BL) hosts, have been suggested to differentiate because of their distinct ecology. The distribution range of BL is within that of HL and bedbugs live mostly on synanthropic bat hosts. This sympatric co-occurrence predicts strong reproductive isolation at the post-copulatory level. RESULTS: We tested the post-copulatory barrier in three BL and three HL populations in reciprocal crosses, using a common-garden blood diet that was novel to both lineages. We excluded pre-copulation isolation mechanisms and studied egg-laying rates after a single mating until the depletion of sperm, and the fitness of the resulting offspring. We found a higher sperm storage capability in BL, likely reflecting the different seasonal availability of HL and BL hosts. We also observed a notable variation in sperm function at the population level within lineages and significant differences in fecundity and offspring fitness between lineages. However, no difference in egg numbers or offspring fitness was observed between within- and between-lineage crosses. CONCLUSIONS: Differences in sperm storage or egg-laying rates between HL and BL that we found did not affect reproductive isolation. Neither did the population-specific variation in sperm function. Overall, our results show no post-copulatory reproductive isolation between the lineages. How genetic differentiation in sympatry is maintained in the absence of a post-copulatory barrier between BL and HL remains to be investigated.

• Keywords
• Ecological speciation, Host adaptation, Host fidelity, Sperm storage,
• Publication type
• Journal Article MeSH

As populations differentiate across geographic or host-association barriers, interpopulation fertility is often a measure of the extent of incipient speciation. The bed bug, Cimex lectularius L., was recently found to form two host-associated lineages within Europe: one found with humans (human-associated, HA) and the other found with bats (bat-associated, BA). No unequivocal evidence of contemporary gene flow between these lineages has been found; however, it is unclear whether this is due to an inability to produce viable "hybrid" offspring. To address this question and determine the extent of compatibility between host-associated lineages, we set up mating crosses among populations of bed bugs based on both their host association (human-HA vs. bat-BA) and geographic origin (North America vs. Europe). Within-population fecundity was significantly higher for all HA populations (>1.7 eggs/day) than for BA populations (<1 egg/day). However, all within-population crosses, regardless of host association, had >92% egg hatch rates. Contrary to previous reports, in all interlineage crosses, successful matings occurred, fertile eggs were oviposited, and the F1 "hybrid" generation was found to be reproductively viable. In addition, we evaluated interpopulation genetic variation in Wolbachia among host-associated lineages. We did not find any clear patterns related to host association, nor did we observe a homogenization of Wolbachia lineages across populations that might explain a breakdown of reproductive incompatibility. These results indicate that while the HA and BA populations of C. lectularius represent genetically differentiated host-associated lineages, possibly undergoing sympatric speciation, this is in its incipient stage as they remain reproductively compatible. Other behavioral, physiological, and/or ecological factors likely maintain host-associated differentiation.

• Keywords
• Cimexlectularius, Wolbachia, host‐associated differentiation, reproduction, speciation,
• Publication type
• Journal Article MeSH

Bed bugs (Cimex lectularius) provide a unique opportunity to understand speciation and host-associated divergence in parasites. Recently, two sympatric but genetically distinct lineages of C. lectularius were identified: one associated with humans and one associated with bats. We investigated two mechanisms that could maintain genetic differentiation in the field: reproductive compatibility (via mating crosses) and aggregation fidelity (via two-choice sheltering assays). Effects were assessed at the intra-lineage level (within human-associated bed bugs), inter-lineage level (between human- and bat-associated bed bugs), and inter-species level (between C. lectularius and Cimex pipistrelli [bat bug]). Contrary to previous reports, bed bugs were found to be reproductively compatible at both the intra- and inter-lineage levels, but not at the inter-species level (although three hybrids were produced, one of which developed into an adult). Lineage- and species-specific aggregation fidelity was only detected in 8% (4 out of 48) of the aggregation fidelity assays run. These results indicate that under laboratory conditions, host-associated lineages of bed bugs are reproductively compatible, and aggregation pheromones are not capable of preventing gene flow between lineages.

• MeSH
• Behavior, Animal physiology   MeSH
• Chi-Square Distribution MeSH
• Reproduction genetics   physiology   MeSH
• Bedbugs genetics   physiology   MeSH
• Gene Flow genetics   physiology   MeSH
• Animals MeSH
• Check Tag
• Male MeSH
• Female MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Research Support, N.I.H., Extramural MeSH
• Research Support, U.S. Gov't, Non-P.H.S. MeSH

The common bed bug Cimex lectularius, has been recently shown to constitute two host races, which are likely in the course of incipient speciation. The human-associated lineage splits from the ancestral bat-associated species deep in the history of modern humans, likely even prior to the Neolithic Period and establishment of the first permanent human settlements. Hybridization experiments between these two lineages show that post-mating reproductive barriers are incomplete due to local variation. As mating takes place in off-host refugia marked by aggregation semiochemicals, the present investigation tested the hypothesis that bed bugs use these semiochemicals to differentiate between refugia marked by bat- and human-associated bed bugs; this would constitute a pre-copulation isolation mechanism. The preference for lineage-specific odors was tested using artificial shelters conditioned by a group of either male or female bed bugs. Adult males were assayed individually in four-choice assays that included two clean unconditioned control shelters. In most assays, bed bugs preferred to rest in conditioned shelters, with no apparent fidelity to shelters conditioned by their specific lineage. However, 51 % of the bat-associated males preferred unconditioned shelters over female-conditioned shelters of either lineage. Thus, bed bugs show no preferences for lineage-specific shelters, strongly suggesting that semiochemicals associated with shelters alone do not function in reproductive isolation.

• Keywords
• Aggregation behavior, Parasites, Pheromones, Pre-copulation reproduction isolation,
• MeSH
• Biological Assay MeSH
• Chiroptera parasitology   MeSH
• Hybridization, Genetic MeSH
• Ectoparasitic Infestations parasitology   veterinary   MeSH
• Humans MeSH
• Odorants analysis   MeSH
• Reproduction MeSH
• Bedbugs classification   genetics   physiology   MeSH
• Animals MeSH
• Check Tag
• Humans MeSH
• Male MeSH
• Female MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH