Reproductive compatibility among populations and host-associated lineages of the common bed bug (Cimex lectularius L.)

Zachary C. DeVries; Richard G. Santangelo; Warren Booth; Christopher G. Lawrence; Ondřej Balvín; Tomáš Bartonička; Coby Schal

doi:10.1002/ece3.6738

Reproductive compatibility among populations and host-associated lineages of the common bed bug (Cimex lectularius L.)

Zachary C. DeVries, Richard G. Santangelo, Warren Booth, Christopher G. Lawrence, Ondřej Balvín, Tomáš Bartonička, Coby Schal

Research output: Contribution to journal › Article › peer-review

1 Scopus citations

Abstract

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.

Original language	English
Pages (from-to)	11090-11099
Number of pages	10
Journal	Ecology and Evolution
Volume	10
Issue number	20
DOIs	https://doi.org/10.1002/ece3.6738
State	Published - Oct 1 2020

Bibliographical note

Funding Information:
We thank Russell Mick for assistance with experimental animals during this study. Funding for this study was provided by the Blanton J. Whitmire Endowment at North Carolina State University, the U.S. Department of Housing and Urban Development Healthy Homes program (NCHHU0017‐13), the Alfred P. Sloan Foundation (2013‐5‐35 MBE), a National Institute of Environmental Health Sciences grant to the Center for Human Health and the Environment (CHHE, P30ES025128), and the National Science Foundation (DEB‐1754394 and DEB‐1754190). ZD was supported in part by the David R. Nimocks Jr. Fellowship and scholarship awards from the Foundation for Agromedicine and Toxicology, Pi Chi Omega, and the Entomological Society of America (Monsanto Research Grant Award, MUVE Scholarship). Additional funding to WB was provided by a Faculty Research Grant awarded by The University of Tulsa and the Oklahoma Center for the Advancement of Science and Technology (HR13‐211). OB and TB were supported by Czech Science Foundation No. 18‐08468J.

Funding Information:
We thank Russell Mick for assistance with experimental animals during this study. Funding for this study was provided by the Blanton J. Whitmire Endowment at North Carolina State University, the U.S. Department of Housing and Urban Development Healthy Homes program (NCHHU0017-13), the Alfred P. Sloan Foundation (2013-5-35 MBE), a National Institute of Environmental Health Sciences grant to the Center for Human Health and the Environment (CHHE, P30ES025128), and the National Science Foundation (DEB-1754394 and DEB-1754190). ZD was supported in part by the David R. Nimocks Jr. Fellowship and scholarship awards from the Foundation for Agromedicine and Toxicology, Pi Chi Omega, and the Entomological Society of America (Monsanto Research Grant Award, MUVE Scholarship). Additional funding to WB was provided by a Faculty Research Grant awarded by The University of Tulsa and the Oklahoma Center for the Advancement of Science and Technology (HR13-211). OB and TB were supported by Czech Science Foundation No. 18-08468J.

Publisher Copyright:
© 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd

Keywords

Cimex lectularius
Wolbachia
host-associated differentiation
reproduction
speciation

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Ecology
Nature and Landscape Conservation

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10.1002/ece3.6738

Cite this

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title = "Reproductive compatibility among populations and host-associated lineages of the common bed bug (Cimex lectularius L.)",

abstract = "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.",

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note = "Funding Information: We thank Russell Mick for assistance with experimental animals during this study. Funding for this study was provided by the Blanton J. Whitmire Endowment at North Carolina State University, the U.S. Department of Housing and Urban Development Healthy Homes program (NCHHU0017‐13), the Alfred P. Sloan Foundation (2013‐5‐35 MBE), a National Institute of Environmental Health Sciences grant to the Center for Human Health and the Environment (CHHE, P30ES025128), and the National Science Foundation (DEB‐1754394 and DEB‐1754190). ZD was supported in part by the David R. Nimocks Jr. Fellowship and scholarship awards from the Foundation for Agromedicine and Toxicology, Pi Chi Omega, and the Entomological Society of America (Monsanto Research Grant Award, MUVE Scholarship). Additional funding to WB was provided by a Faculty Research Grant awarded by The University of Tulsa and the Oklahoma Center for the Advancement of Science and Technology (HR13‐211). OB and TB were supported by Czech Science Foundation No. 18‐08468J. Funding Information: We thank Russell Mick for assistance with experimental animals during this study. Funding for this study was provided by the Blanton J. Whitmire Endowment at North Carolina State University, the U.S. Department of Housing and Urban Development Healthy Homes program (NCHHU0017-13), the Alfred P. Sloan Foundation (2013-5-35 MBE), a National Institute of Environmental Health Sciences grant to the Center for Human Health and the Environment (CHHE, P30ES025128), and the National Science Foundation (DEB-1754394 and DEB-1754190). ZD was supported in part by the David R. Nimocks Jr. Fellowship and scholarship awards from the Foundation for Agromedicine and Toxicology, Pi Chi Omega, and the Entomological Society of America (Monsanto Research Grant Award, MUVE Scholarship). Additional funding to WB was provided by a Faculty Research Grant awarded by The University of Tulsa and the Oklahoma Center for the Advancement of Science and Technology (HR13-211). OB and TB were supported by Czech Science Foundation No. 18-08468J. Publisher Copyright: {\textcopyright} 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd",

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N2 - 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.

AB - 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.

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Reproductive compatibility among populations and host-associated lineages of the common bed bug (Cimex lectularius L.)

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

Access to Document

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