Warp-speed adaptation to novel hosts after 300 generations of enforced dietary specialisation in the seed beetle Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae)

Thomas Price, Aoife Leonard, Lesley T Lancaster (Corresponding Author)

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Abstract

Herbivorous insects are often highly specialised, likely due to trade-offs in fitness on alternative host species. However, some pest insects are extremely adaptable and readily adopt novel hosts, sometimes causing rapid expansion of their host range as they spread from their original host and geographic origin. The genetic basis of this phenomenon is poorly understood, limiting our ability to predict or mitigate global insect pest outbreaks. We investigated the trajectory of early adaptation to novel hosts in a regionally-specialised global crop pest species (the cowpea seed beetle Callosobruchus maculatus). After experimentally-enforced dietary specialisation for nearly 300 generations, we measured changes in fitness over the first 5 generations of adaptation to 6 novel hosts. Of these, C. maculatus reproduced successfully on all but one, with reduced fitness observed on three hosts in the first generation. Loss of fitness was followed by very rapid, decelerating increases in fitness over the first 1-5 generations, resulting in comparable levels of population fitness to that observed on the original host after 5 generations. Heritability of fitness on novel hosts was high. Adaptation occurred primarily via changes in behavioural and phenological traits, and never via changes in offspring survival to adulthood, despite high heritability for this trait. These results suggest that C. maculatus possesses ample additive genetic variation for very rapid host shifts, despite a prolonged period of enforced specialization, and also suggest that some previously-inferred environmental maternal effects on host use may in part actually represent (rapidly) evolved changes. We highlight the need to examine in more detail the genetic architecture facilitating retention of high additive genetic variation for host shifts in extremely adaptable global crop pests.
Original languageEnglish
Pages (from-to)257-266
Number of pages10
JournalEuropean Journal of Entomology
Volume114
Early online date26 May 2017
DOIs
Publication statusPublished - 2017

Fingerprint

Callosobruchus maculatus
Bruchidae
Chrysomelidae
Coleoptera
plant pests
insect pests
heritability
alternative hosts
genetic variation
phytophagous insects
maternal effect
adulthood
cowpeas
host range
provenance
trajectories

Keywords

  • emerging crop pests
  • host shifts
  • genetic variation
  • adaptation trajectory
  • evolvability
  • experimental evolution
  • quasi-natural selection
  • heritability

Cite this

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title = "Warp-speed adaptation to novel hosts after 300 generations of enforced dietary specialisation in the seed beetle Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae)",
abstract = "Herbivorous insects are often highly specialised, likely due to trade-offs in fitness on alternative host species. However, some pest insects are extremely adaptable and readily adopt novel hosts, sometimes causing rapid expansion of their host range as they spread from their original host and geographic origin. The genetic basis of this phenomenon is poorly understood, limiting our ability to predict or mitigate global insect pest outbreaks. We investigated the trajectory of early adaptation to novel hosts in a regionally-specialised global crop pest species (the cowpea seed beetle Callosobruchus maculatus). After experimentally-enforced dietary specialisation for nearly 300 generations, we measured changes in fitness over the first 5 generations of adaptation to 6 novel hosts. Of these, C. maculatus reproduced successfully on all but one, with reduced fitness observed on three hosts in the first generation. Loss of fitness was followed by very rapid, decelerating increases in fitness over the first 1-5 generations, resulting in comparable levels of population fitness to that observed on the original host after 5 generations. Heritability of fitness on novel hosts was high. Adaptation occurred primarily via changes in behavioural and phenological traits, and never via changes in offspring survival to adulthood, despite high heritability for this trait. These results suggest that C. maculatus possesses ample additive genetic variation for very rapid host shifts, despite a prolonged period of enforced specialization, and also suggest that some previously-inferred environmental maternal effects on host use may in part actually represent (rapidly) evolved changes. We highlight the need to examine in more detail the genetic architecture facilitating retention of high additive genetic variation for host shifts in extremely adaptable global crop pests.",
keywords = "emerging crop pests, host shifts, genetic variation, adaptation trajectory, evolvability, experimental evolution , quasi-natural selection, heritability",
author = "Thomas Price and Aoife Leonard and Lancaster, {Lesley T}",
note = "Thank you to Paul Eady for providing C. maculatus to initiate our laboratory population and advice on rearing them. The study was funded by the University of Aberdeen core teaching funds (honours project budget to TP), and by a doctoral training grant to AL from the BBSRC-EastBio doctoral training partnership",
year = "2017",
doi = "10.14411/eje.2017.031",
language = "English",
volume = "114",
pages = "257--266",
journal = "European Journal of Entomology",
issn = "1802-8829",
publisher = "Czech Academy of Sciences",

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T1 - Warp-speed adaptation to novel hosts after 300 generations of enforced dietary specialisation in the seed beetle Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae)

AU - Price, Thomas

AU - Leonard, Aoife

AU - Lancaster, Lesley T

N1 - Thank you to Paul Eady for providing C. maculatus to initiate our laboratory population and advice on rearing them. The study was funded by the University of Aberdeen core teaching funds (honours project budget to TP), and by a doctoral training grant to AL from the BBSRC-EastBio doctoral training partnership

PY - 2017

Y1 - 2017

N2 - Herbivorous insects are often highly specialised, likely due to trade-offs in fitness on alternative host species. However, some pest insects are extremely adaptable and readily adopt novel hosts, sometimes causing rapid expansion of their host range as they spread from their original host and geographic origin. The genetic basis of this phenomenon is poorly understood, limiting our ability to predict or mitigate global insect pest outbreaks. We investigated the trajectory of early adaptation to novel hosts in a regionally-specialised global crop pest species (the cowpea seed beetle Callosobruchus maculatus). After experimentally-enforced dietary specialisation for nearly 300 generations, we measured changes in fitness over the first 5 generations of adaptation to 6 novel hosts. Of these, C. maculatus reproduced successfully on all but one, with reduced fitness observed on three hosts in the first generation. Loss of fitness was followed by very rapid, decelerating increases in fitness over the first 1-5 generations, resulting in comparable levels of population fitness to that observed on the original host after 5 generations. Heritability of fitness on novel hosts was high. Adaptation occurred primarily via changes in behavioural and phenological traits, and never via changes in offspring survival to adulthood, despite high heritability for this trait. These results suggest that C. maculatus possesses ample additive genetic variation for very rapid host shifts, despite a prolonged period of enforced specialization, and also suggest that some previously-inferred environmental maternal effects on host use may in part actually represent (rapidly) evolved changes. We highlight the need to examine in more detail the genetic architecture facilitating retention of high additive genetic variation for host shifts in extremely adaptable global crop pests.

AB - Herbivorous insects are often highly specialised, likely due to trade-offs in fitness on alternative host species. However, some pest insects are extremely adaptable and readily adopt novel hosts, sometimes causing rapid expansion of their host range as they spread from their original host and geographic origin. The genetic basis of this phenomenon is poorly understood, limiting our ability to predict or mitigate global insect pest outbreaks. We investigated the trajectory of early adaptation to novel hosts in a regionally-specialised global crop pest species (the cowpea seed beetle Callosobruchus maculatus). After experimentally-enforced dietary specialisation for nearly 300 generations, we measured changes in fitness over the first 5 generations of adaptation to 6 novel hosts. Of these, C. maculatus reproduced successfully on all but one, with reduced fitness observed on three hosts in the first generation. Loss of fitness was followed by very rapid, decelerating increases in fitness over the first 1-5 generations, resulting in comparable levels of population fitness to that observed on the original host after 5 generations. Heritability of fitness on novel hosts was high. Adaptation occurred primarily via changes in behavioural and phenological traits, and never via changes in offspring survival to adulthood, despite high heritability for this trait. These results suggest that C. maculatus possesses ample additive genetic variation for very rapid host shifts, despite a prolonged period of enforced specialization, and also suggest that some previously-inferred environmental maternal effects on host use may in part actually represent (rapidly) evolved changes. We highlight the need to examine in more detail the genetic architecture facilitating retention of high additive genetic variation for host shifts in extremely adaptable global crop pests.

KW - emerging crop pests

KW - host shifts

KW - genetic variation

KW - adaptation trajectory

KW - evolvability

KW - experimental evolution

KW - quasi-natural selection

KW - heritability

U2 - 10.14411/eje.2017.031

DO - 10.14411/eje.2017.031

M3 - Article

VL - 114

SP - 257

EP - 266

JO - European Journal of Entomology

JF - European Journal of Entomology

SN - 1802-8829

ER -