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

Erica L. Larson, Margaret M. Brassil, Jonathan Maslan, Danielle Juárez, Flordeliza Lilagan, Hallie Tipton, Andrew Schweitzer, Joe Skillman, Kirsten Monsen, Merrill A. Peterson

Research output: Contribution to journalArticle

Abstract

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 of PMPZ barriers 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 auratus and C. 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 in C. cobaltinus and extended to heterospecific matings. We found that PMPZ barriers greatly limited hybrid production by C. auratus females with moderate heterospecific mating frequencies, but that their effectiveness diminished at higher heterospecific mating frequencies. In contrast, there was no evidence for PMPZ barriers in C. cobaltinus females 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 the Chrysochus hybrid 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.

Original languageEnglish
Pages (from-to)900-912
Number of pages13
JournalJournal of Evolutionary Biology
Volume32
Issue number9
DOIs
StatePublished - 1 Sep 2019

Fingerprint

mating frequency
hybrid zone
multiple mating
reproductive isolation
introgression
sperm
fecundity
relative abundance
beetle
effect
Chrysomelidae
spermatozoa

Keywords

  • conspecific sperm precedence
  • cryptic reproductive barriers
  • hybrid zone
  • hybridization frequency
  • post-mating prezygotic barriers
  • relative abundance
  • speciation

Cite this

Larson, E. L., Brassil, M. M., Maslan, J., Juárez, D., Lilagan, F., Tipton, H., ... Peterson, M. A. (2019). The effects of heterospecific mating frequency on the strength of cryptic reproductive barriers. Journal of Evolutionary Biology, 32(9), 900-912. https://doi.org/10.1111/jeb.13495
Larson, Erica L. ; Brassil, Margaret M. ; Maslan, Jonathan ; Juárez, Danielle ; Lilagan, Flordeliza ; Tipton, Hallie ; Schweitzer, Andrew ; Skillman, Joe ; Monsen, Kirsten ; Peterson, Merrill A. / The effects of heterospecific mating frequency on the strength of cryptic reproductive barriers. In: Journal of Evolutionary Biology. 2019 ; Vol. 32, No. 9. pp. 900-912.
@article{4347cfec8c7940929fa54c79564b378b,
title = "The effects of heterospecific mating frequency on the strength of cryptic reproductive barriers",
abstract = "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 of PMPZ barriers 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 auratus and C. 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 in C. cobaltinus and extended to heterospecific matings. We found that PMPZ barriers greatly limited hybrid production by C. auratus females with moderate heterospecific mating frequencies, but that their effectiveness diminished at higher heterospecific mating frequencies. In contrast, there was no evidence for PMPZ barriers in C. cobaltinus females 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 the Chrysochus hybrid 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.",
keywords = "conspecific sperm precedence, cryptic reproductive barriers, hybrid zone, hybridization frequency, post-mating prezygotic barriers, relative abundance, speciation",
author = "Larson, {Erica L.} and Brassil, {Margaret M.} and Jonathan Maslan and Danielle Ju{\'a}rez and Flordeliza Lilagan and Hallie Tipton and Andrew Schweitzer and Joe Skillman and Kirsten Monsen and Peterson, {Merrill A.}",
year = "2019",
month = "9",
day = "1",
doi = "10.1111/jeb.13495",
language = "English",
volume = "32",
pages = "900--912",
journal = "Journal of Evolutionary Biology",
issn = "1010-061X",
publisher = "Wiley-Blackwell Publishing Ltd",
number = "9",

}

Larson, EL, Brassil, MM, Maslan, J, Juárez, D, Lilagan, F, Tipton, H, Schweitzer, A, Skillman, J, Monsen, K & Peterson, MA 2019, 'The effects of heterospecific mating frequency on the strength of cryptic reproductive barriers', Journal of Evolutionary Biology, vol. 32, no. 9, pp. 900-912. https://doi.org/10.1111/jeb.13495

The effects of heterospecific mating frequency on the strength of cryptic reproductive barriers. / Larson, Erica L.; Brassil, Margaret M.; Maslan, Jonathan; Juárez, Danielle; Lilagan, Flordeliza; Tipton, Hallie; Schweitzer, Andrew; Skillman, Joe; Monsen, Kirsten; Peterson, Merrill A.

In: Journal of Evolutionary Biology, Vol. 32, No. 9, 01.09.2019, p. 900-912.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The effects of heterospecific mating frequency on the strength of cryptic reproductive barriers

AU - Larson, Erica L.

AU - Brassil, Margaret M.

AU - Maslan, Jonathan

AU - Juárez, Danielle

AU - Lilagan, Flordeliza

AU - Tipton, Hallie

AU - Schweitzer, Andrew

AU - Skillman, Joe

AU - Monsen, Kirsten

AU - Peterson, Merrill A.

PY - 2019/9/1

Y1 - 2019/9/1

N2 - 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 of PMPZ barriers 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 auratus and C. 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 in C. cobaltinus and extended to heterospecific matings. We found that PMPZ barriers greatly limited hybrid production by C. auratus females with moderate heterospecific mating frequencies, but that their effectiveness diminished at higher heterospecific mating frequencies. In contrast, there was no evidence for PMPZ barriers in C. cobaltinus females 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 the Chrysochus hybrid 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.

AB - 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 of PMPZ barriers 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 auratus and C. 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 in C. cobaltinus and extended to heterospecific matings. We found that PMPZ barriers greatly limited hybrid production by C. auratus females with moderate heterospecific mating frequencies, but that their effectiveness diminished at higher heterospecific mating frequencies. In contrast, there was no evidence for PMPZ barriers in C. cobaltinus females 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 the Chrysochus hybrid 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.

KW - conspecific sperm precedence

KW - cryptic reproductive barriers

KW - hybrid zone

KW - hybridization frequency

KW - post-mating prezygotic barriers

KW - relative abundance

KW - speciation

UR - http://www.scopus.com/inward/record.url?scp=85067431557&partnerID=8YFLogxK

U2 - 10.1111/jeb.13495

DO - 10.1111/jeb.13495

M3 - Article

C2 - 31162735

AN - SCOPUS:85067431557

VL - 32

SP - 900

EP - 912

JO - Journal of Evolutionary Biology

JF - Journal of Evolutionary Biology

SN - 1010-061X

IS - 9

ER -