Mating rate and fitness in female bean weevils

Females of most animal taxa mate with several males during their lifespan. Yet our understanding of the ultimate causes of polyandry is incomplete. For example, it is not clear if and in what sense female mating rates are optimal. Most female insects are thought to maximize their fitness by mating at an intermediate rate, but it has been suggested that two alternative fitness peaks may be observed if multiple costs and benefits interact in determining the relationship between mating rate and fitness. We studied the relationship between female fitness and mating rate in the bean weevil, Callosobruchus maculatus (Coleoptera: Bruchidae), a species in which several distinct direct effects of mating to females have been reported. Our results show that female fitness, measured as lifetime offspring production, is lowest at an intermediate mating rate. We suggest that this pattern is the result of multiple direct benefits to mating (e.g., sperm replenishment and hydration/nutrition effects) in combination with significant direct costs to mating (e.g., injury from male genitalia). Females mating at low rates may efficiently minimize the costs of mating, whereas females mating at high rates instead may maximize the benefits of mating. If common, the existence of bimodal relationships between female mating rate and fitness may help explain the large intra- and interspecific variation in the degree of polyandry often seen in insects. Copyright 2005.

[1]  A. Das,et al.  Isolation of the two paragonial substances deposited into the spermatophores ofAcanthoscelides obtectus (Coleoptera, Bruchidae) , 1980, Experientia.

[2]  C. Fricke,et al.  Divergence in replicated phylogenies: the evolution of partial post‐mating prezygotic isolation in bean weevils , 2004, Journal of evolutionary biology.

[3]  P. Eady,et al.  The Effect of Single, Double, and Triple Matings on the Lifetime Fecundity of Callosobruchus analis and Callosobruchus maculatus (Coleoptera: Bruchidae) , 1999, Journal of Insect Behavior.

[4]  C. Fox The influence of maternal age and mating frequency on egg size and offspring performance in Callosobruchus maculatus (Coleoptera: Bruchidae) , 1993, Oecologia.

[5]  C. Wiklund,et al.  Monandry and polyandry as alternative lifestyles in a butterfly , 2002 .

[6]  C. Wiklund,et al.  Sexual conflict and cooperation in butterfly reproduction: a comparative study of polyandry and female fitness , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  S. Gavrilets,et al.  The evolution of female mate choice by sexual conflict , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[8]  H. S. Crudgington Sexual conflict in the bean weevil, Callosobruchus maculatus , 2001 .

[9]  P. Eady,et al.  COPULATING WITH MULTIPLE MATES ENHANCES FEMALE FECUNDITY BUT NOT EGG‐TO‐ADULT SURVIVAL IN THE BRUCHID BEETLE CALLOSOBRUCHUS MACULATUS , 2000, Evolution; international journal of organic evolution.

[10]  M. Siva-jothy,et al.  Genital damage, kicking and early death , 2000, Nature.

[11]  L. Keller,et al.  How Males Can Gain by Harming Their Mates: Sexual Conflict, Seminal Toxins, and the Cost of Mating , 2000, The American Naturalist.

[12]  G. Arnqvist,et al.  The evolution of polyandry: multiple mating and female fitness in insects , 2000, Animal Behaviour.

[13]  P. Eady,et al.  Spermatophore size and mate fecundity in the bruchid beetle Callosobruchus maculatus , 2000 .

[14]  M. Petrie,et al.  Why do females mate multiply? A review of the genetic benefits , 2000, Biological reviews of the Cambridge Philosophical Society.

[15]  K. Takakura Active female courtship behavior and male nutritional contribution to female fecundity in Bruchidius dorsalis (Fahraeus) (Coleoptera: Bruchidae) , 1999, Researches on Population Ecology.

[16]  S. Sakaluk,et al.  Hydration benefits to courtship feeding in crickets , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[17]  C. Fox,et al.  The effect of male mating history on paternal investment, fecundity and female remating in the seed beetle Callosobruchus maculatus , 1999 .

[18]  L. Partridge,et al.  Interactions of mating, egg production and death rates in females of the Mediterranean fruitfly, Ceratitis capitata , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[19]  C. Fox,et al.  Genetic variation in paternal investment in a seed beetle , 1998, Animal Behaviour.

[20]  M. Siva-jothy,et al.  Decreased immune response as a proximate cost of copulation and oviposition in a damselfly , 1998 .

[21]  K. Vahed The function of nuptial feeding in insects: a review of empirical studies , 1998 .

[22]  W. Rice,et al.  PERSPECTIVE: CHASE‐AWAY SEXUAL SELECTION: ANTAGONISTIC SEDUCTION VERSUS RESISTANCE , 1998, Evolution; international journal of organic evolution.

[23]  G. Arnqvist,et al.  Sexual Conflict and the Energetic Costs of Mating and Mate Choice in Water Striders , 1998, The American Naturalist.

[24]  M. Tatar,et al.  Nutrition Mediates Reproductive Trade‐Offs with Age‐Specific Mortality in the Beetle Callosobruchus Maculatus , 1995 .

[25]  G. Hurst,et al.  Sexually transmitted disease in a promiscuous insect, Adalia bipunctata , 1995 .

[26]  James R. Carey,et al.  LONG‐TERM COST OF REPRODUCTION WITH AND WITHOUT ACCELERATED SENESCENCE IN CALLOSOBRUCHUS MACULATUS: ANALYSIS OF AGE‐SPECIFIC MORTALITY , 1993, Evolution; international journal of organic evolution.

[27]  L. Partridge,et al.  No reduction in the cost of mating for Drosophila melanogaster females mating with spermless males , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[28]  C. Fox Multiple mating, lifetime fecundity and female mortality of the bruchid beetle, Callosobruchus maculatus (Coleoptera: Bruchidae) , 1993 .

[29]  G. Arnqvist Multiple mating in a water strider: mutual benefits or intersexual conflict? , 1989, Animal Behaviour.

[30]  S. Wing Cost of Mating for Female Insects: Risk of Predation in Photinus collustrans (Coleoptera: Lampyridae) , 1988, The American Naturalist.

[31]  J. Huignard,et al.  Transfer of male secretions from the spermatophore to the female insect in Caryedon serratus (Ol.): Analysis of the possible trophic role of these secretions , 1987 .

[32]  M. Wade,et al.  THE EVOLUTION OF INSECT MATING SYSTEMS. , 1984, Evolution; international journal of organic evolution.

[33]  J. Huignard Transfer and fate of male secretions deposited in the spermatophore of females of Acanthoscelides obtectus Say (Coleoptera Bruchidae) , 1983 .

[34]  B. Leroi Feeding, Longevity and Reproduction of Adults of Acanthoscelides Obtectus Say in Laboratory Conditions , 1981 .

[35]  V. Labeyrie The Ecology of Bruchids Attacking Legumes (Pulses) , 1981, Series Entomologica.

[36]  M. Daly The Cost of Mating , 1978, The American Naturalist.