Sperm ecology, sexual co-evolution and evolutionary diversification

Research Question

How does environmental sperm damage (sperm ecology) and the co-evolution between the sexes cause rapid evolutionary change (speciation, trait evolution and polymorphism)?

We address this question using insect model systems (bedbugs, Drosophila, crickets) and look at variation in cell biology, proteins, physiology, behaviour and morphology.

Sperm ecology: the sperm phenotype and its evolutionary consequences

All cells decrease in function over time (senescence) and sperm are no exception. Fertilisation and zygote viability critically depend on the environmental damage that sperm cells have incurred before fertilisation. Because sperm senescence differs across environments, male and female adaptations to prevent fertilisation with such environmentally damaged, i.e. aged, sperm will also differ. We investigate this naturally, not sexually selected, component of sperm function for the following (sperm) environments: microbes, oxidative stress and the immune system (Reinhardt 2007 Q Rev Biol 82:375// Otti et al. 2009 Am Nat 174, 292) as well as oxygen, CO2 and diet.

Co-evolution between the sexes: Why is reproduction so complicated?

In bedbugs we study a fast evolutionary ping-pong play: Male bedbugs copulate by piercing the female abdomen wall to which females respond by evolving a novel biomaterial. Males also transmit microbes during mating against which females evolve a new immune organ. Males mate when females are unable to resist mating (situation exploitation) to which females will respond by… (Reinhardt et al. 2003 Proc B 270, 2371// 2009 Evolution 63, 29 // 2009 PNAS 106, 21743).

Genitalia evolution

Genitalia show a greater diversity between species than other morphological characters. Why? Sexual selection by female choice for males with different genitalia types has been suggested. Yet, if genitalia were honest sexual signals we should expect large variation between males. However, male genitalia show small variation within a species – so small that genitalia are the key identification feature for many animals. Genitalia variation may also be caused by natural selection and pleiotropy (Reinhardt 2010 Genetica 138, 119). Bedbugs are an interesting study system because they defeat current theory on genitalia evolution: 1) Male genitalia do not covary with female genitalia. 2) In species in which males mate with other males, males have evolved female-like genitalia. In turn, some females mimic the male form of female genitalia (Reinhardt et al. 2007 Am Nat 170, 931).

Group Members

In Sheffield

Toby Fountain: Population Genetics of Bedbugs

Dr Oliver Otti: Sexual conflict and reproductive immunity in the bedbug

In Tübingen

Klaus Reinhardt

Dr Jessica Abbott: Genotype x diet interaction effects on sperm function

Dr Ralph Dobler: Genotype x environment interaction effects on Sperm Function: oxygen, CO2

Recent and Current Funding

VolkswagenStiftung: Environment, Sperm Function and Evolution, 2010 - 2013

Royal Society of London: Female Transcriptome Responses to Sperm (454 Sequencing), 2009-2010

NERC: Evolutionary Consequences of Sperm Ageing, 2006-2010

NBAF: Population Genetics of Bedbugs, 2010-2012

Key Publications

Ribou, A.-C. & Reinhardt, K. (2012). Reduced metabolic rate and oxygen radicals production in stored insect sperm. Proc. R. Soc. B 279: 2196-2203

 

Reinhardt, K. 2010. Natural selection and genital variation: a role for the environment, parasites and sperm ageing? Genetica 138:119–127

 

Reinhardt, K., Naylor, R. & Siva-Jothy, M. T. Ejaculate components delay reproductive senescence while elevating female reproductive rate in an insect. PNAS 106:21743-21747

 

Reinhardt, K., Naylor, R. & Siva-Jothy, M. T. 2009 Situation exploitation: higher male mating success when female resistance is reduced by feeding. Evolution 63: 29-39

 

Reinhardt, K., Wong, C. H., Georgiou, A. S. 2009. Seminal fluid proteins in the bed bug, Cimex lectularius, detected using two-dimensional gel electrophoresis and mass spectrometry. Parasitology 136: 283-292

 

Otti, O., Naylor, R., Siva-Jothy, M.T. & Reinhardt, K. 2009. Bacteriolytic activity in the ejaculate of an insect. American Naturalist 174:292-295

 

Reinhardt, K. 2007. Evolutionary consequences of sperm cell aging. Quarterly Review of Biology 82: 375-393

 

Reinhardt, K., Harney, E., Naylor, R, Gorb, S. & Siva-Jothy, M. T. 2007. Female-limited genitalia polymorphism in a traumatically inseminating insect. American Naturalist 170: 931-935

 

Reinhardt, K. & Siva-Jothy, M. T. 2007. Biology of bed bugs (Cimicidae). Annual Review of Entomology 52: 351-374

 

Reinhardt, K. & Siva-Jothy, M. T. 2005. An advantage for young sperm in the house cricket Acheta domesticus. American Naturalist 165: 718-723

 

Reinhardt, K., Naylor, R. & Siva-Jothy, M. T. 2003. Reducing a cost of traumatic insemination: female bed bugs evolve a unique organ. Proc. R. Soc. Lond. B 270: 2371-2375.

Collaborators

Dr Anne-Cecile Ribou, Perpignan – Oxidative stress production in sperm

Prof. Janis Antonovics, Virginia  – Sperm - Microbe Interactions

Prof. Karsten König, Saarbrücken - Sperm metabolic mapping: fluorescence lifetime imaging (FLIM)

Dr H Rundle, Ottawa – Experimental evolution of Drosophila

Dr Ted Morrow in Uppsala – A phylogeny of bedbugs

Dr Ted Morrow in Uppsala – G x interaction effects on sperm function

Dr Steffen Roth in Bergen – A phylogeny of bedbugs

Prof. Mike Siva-Jothy in Sheffield – A phylogeny of bedbugs

Prof Stanislav Gorb, Kiel - A new biomaterial in the genitalia of female bed bugs

Prof Stanislav Gorb, Kiel - Tarsal attachment structures in the Cimicidae

Prof. Robert Dwyer-Joyce, Sheffield - A material that prevents insect walking

Dr J Samietz, Richterswil - Thermal ecology of haematophagy