Separating two tightly linked species-defining phenotypes in Bactrocera with hybrid recombinant analysis

Heng Lin Yeap; Siu Fai Lee; Freya Robinson; Roslyn G Mourant; John A Sved; Marianne Frommer; Alexie Papanicolaou; Owain R Edwards; John G Oakeshott

doi:10.1186/s12863-020-00936-1

Separating two tightly linked species-defining phenotypes in Bactrocera with hybrid recombinant analysis

BMC Genet. 2020 Dec 18;21(Suppl 2):132. doi: 10.1186/s12863-020-00936-1.

Authors

Heng Lin Yeap¹, Siu Fai Lee^{2

3}, Freya Robinson², Roslyn G Mourant², John A Sved⁴, Marianne Frommer⁴, Alexie Papanicolaou⁵, Owain R Edwards^{2

3}, John G Oakeshott^{2

3}

Affiliations

¹ CSIRO Land and Water, Black Mountain, Canberra, ACT, 2601, Australia. henglin.yeap@csiro.au.
² CSIRO Land and Water, Black Mountain, Canberra, ACT, 2601, Australia.
³ Applied BioSciences, Macquarie University, Macquarie Park, Sydney, NSW, 2109, Australia.
⁴ School of Biological, Earth and Environmental Sciences, University of New South Wales, Kensington, Sydney, NSW, 2052, Australia.
⁵ Hawkesbury Institute for the Environment, Western Sydney University, Richmond, Sydney, NSW, 2753, Australia.

Abstract

Background: Bactrocera tryoni and Bactrocera neohumeralis mate asynchronously; the former mates exclusively around dusk while the latter mates during the day. The two species also differ in the colour of the post-pronotal lobe (callus), which is predominantly yellow in B. tryoni and brown in B. neohumeralis. We have examined the genetic relationship between the two characters in hybrids, backcrosses and multigeneration hybrid progeny.

Results: Our analysis of the mating time of the parental species revealed that while B. tryoni mate exclusively at dusk, B. neohumeralis females pair with B. neohumeralis males during the day and with B. tryoni males at dusk. We found considerable variance in mating time and callus colour among hybrid backcross individuals of both sexes but there was a strong although not invariant trend for callus colour to co-segregate with mating time in both sexes. To genetically separate these two phenotypes we allowed the interspecific F1 hybrids to propagate for 25 generations (F25) without selection for mating time or callus colour, finding that the advanced hybrid population had moved towards B. tryoni phenotypes for both traits. Selection for day mating in replicate lines at F25 resulted in significant phenotypic shifts in both traits towards B. neohumeralis phenotypes in F26. However, we were unable to completely recover the mating time profile of B. neohumeralis and relaxation of selection for day mating led to a shift back towards dusk mating, but not yellow callus colour, by F35.

Conclusion: We conclude that the inheritance of the two major species-defining traits is separable but tightly linked and involves more than one gene in each case. It also appears that laboratory conditions select for the B. tryoni phenotypes for mating time. We discuss our findings in relation to speciation theory and the likely effects of domestication during the generation of mass release strains for sterile insect control programmes.

Keywords: BACKCROSS; Bactrocera neohumeralis; Bactrocera tryoni; Callus colour; Hybridisation; Mating time; Recombination; Selection.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Crosses, Genetic
Female
Genetic Linkage
Hybridization, Genetic
Inheritance Patterns
Male
Phenotype
Photoperiod*
Sexual Behavior, Animal*
Tephritidae / classification*
Tephritidae / physiology*