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Male-female Coevolution in Bruchid seed beetles
Uppsala universitet.
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Male-female coevolution is at the heart of biology. It is responsible for much of the diversity we see in behaviour and morphology, and it is thought to be an important engine of speciation. The pattern of intersexual coevolution is well established in many taxa, yet understanding of the processes responsible for male-female coevolution remains incomplete. By studying interspecific variation within a closely related group of species, we can gain important information about how traits and behaviours have evolved. In the work done for this thesis, we studied a group of seed beetle species. Our results show that male-female coevolution has been a strong force in shaping both behaviour and morphological traits that are associated with mating and reproduction such as, morphology of male and female genitalia and remating behaviour. The evolution of harmful male genitalia has often been suggested to be a product of sexually antagonistic coevolution, but understanding of these extraordinary adaptations is limited. By combining comparative and experimental methods we show that as seed beetle males evolve more spiny genitalia, harm to females is elevated. We provide evidence for the correlated evolution between these antagonistic adaptations in males, and a female counter adaptation (the amount of connective tissue in the copulatory duct). We also demonstrate that imbalance of relative armament of the sexes affects evolution of the costs and benefits of reproduction. As males evolve genitalia that are more harmful relative to the level of female counteradaptation, costs associated with mating for females increase and population fitness is depressed. Our results unveil a coevolutionary arms race between the sexes and are consistent with a proposed link between sexual conflict, species’ viability and the risk of extinction.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis , 2009. , 38 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 614
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-61566ISBN: 978-91-554-7444-7 (print)OAI: oai:DiVA.org:su-61566DiVA: diva2:436337
Public defence
(English)
Opponent
Supervisors
Available from: 2011-08-31 Created: 2011-08-23 Last updated: 2011-08-31Bibliographically approved
List of papers
1. Evolutionary diversification of the bean beetle genus Callosobruchus (Coleoptera: Bruchidae): Traits associated with stored-product pest status
Open this publication in new window or tab >>Evolutionary diversification of the bean beetle genus Callosobruchus (Coleoptera: Bruchidae): Traits associated with stored-product pest status
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2006 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 15, no 12, 3541-3551 p.Article in journal (Refereed) Published
Abstract [en]

Despite the fact that many plant-feeding insects are pests, little effort has been paid to elucidating key evolutionary trait transitions that allow taxa to acquire or lose pest status. A large proportion of species in the genus Callosobruchus are economically important pests of stored, dry post-harvest beans of the tribe Phaseoleae. However, the evolution of this feeding habit is poorly understood. Here, we present a reconstruction of the phylogeny of the Asian and African Callosobruchus based on three mitochondrial genes, and assess which traits have been associated with the evolutionary origin or loss of ability to reproduce on dry beans. Our phylogenetic analysis showed that species group into the chinensis and the maculatus clades, which are also supported by genital morphology, and an additional paraphyletic group. Ancestral ability to use dry beans has been lost in the chinensis clade but acquired again in C. chinensis. Dry-bean use and host-plant use were both phylogenetically constrained and transitions in the two were significantly correlated. Host shifts from the subtribe Phaseolinae to Cajaninae were more common than the reverse and were more likely in species using young beans. Ability to use dry beans was more likely gained when using Phaseolinae hosts and promoted habitat shifts from tropical to temperate regions. Adaptation to arid climate was associated with ability to reproduce on dry beans and on Phaseolinae. Thus, our analysis suggests that physiological adaptations to arid season and to Phaseolinae hosts both render beetles predisposed to become pests of cultivated beans.

Keyword
Bayesian inference, COI and COII, Fabaceae, host-plant shift, plant-herbivore interactions, Wolbachia
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-61559 (URN)10.1111/j.1365-294X.2006.03030.x (DOI)
Available from: 2011-08-23 Created: 2011-08-23 Last updated: 2017-12-08Bibliographically approved
2.
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3. Interspecific variation in ejaculate allocation and associated effects on female fitness in seed beetles
Open this publication in new window or tab >>Interspecific variation in ejaculate allocation and associated effects on female fitness in seed beetles
2008 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 21, no 2, 461-470 p.Article in journal (Refereed) Published
Abstract [en]

When ejaculates are costly to produce, males are expected to allocate their ejaculate resources over successive matings in a manner that optimises their reproductive success. Theory predicts that two factors should affect optimal ejaculate allocation: the sperm competition regime and variation in female fecundity. In seed beetles (Bruchidae), ejaculates vary in size across species from weighing a few, up to as much as twelve percent, of male body weight. Ejaculates in this group contain not only sperm but also a range of additional substances and it has been proposed that females gain benefits from receiving large ejaculates. Male ejaculate allocation may thus affect female fitness and, indirectly, his own reproductive output. Here, we first measured how males allocate ejaculates over successive matings in seven seed beetle species. We then assessed how this allocation affected female fitness. We found that ejaculate weight drops dramatically over successive matings in some species but not in others. This interspecific variation in ejaculate allocation pattern was matched with extensive variation in the effects of ejaculate allocation on female fitness. Species varied both in terms of the size of the effect of male mating history on female fitness and in terms of which female fitness components were affected. In summary, despite the fact that the species included in this study are closely related, interspecific variation in ejaculate allocation patterns and their effects on female fitness was remarkably large. We discuss the possible causes of this variation and its implications for male-female coevolution.

Keyword
acessory gland products, Callosobruchus, nuptial gifts, sperm allocation
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-61563 (URN)10.1111/j.1420-9101.2007.01493.x (DOI)
Available from: 2011-08-23 Created: 2011-08-23 Last updated: 2017-12-08Bibliographically approved
4. Correlated evolution between male ejacualte allocation and female remating behaviour in seed beetles (Bruchidae)
Open this publication in new window or tab >>Correlated evolution between male ejacualte allocation and female remating behaviour in seed beetles (Bruchidae)
2008 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 21, no 2, 471-479 p.Article in journal (Refereed) Published
Abstract [en]

The pattern with which males allocate their ejaculate resources is at the heart of postmating sexual selection, and theory suggests that female remating rate is key in determining the selective regime under which male ejaculate traits evolve. Intraspecific studies have shown that males are able to adaptively allocate ejaculates according to the intensity of sperm competition, but observational data does not allow explicitly comparative tests of theory in this field. Using a group of seed beetles as a model system, we analyzed experimental quantifications of a suite of relevant male and female traits and behaviors in a phylogenetic comparative framework. We found a strongly and positively correlated evolution between the weight of males’ first ejaculate and the rate at which ejaculate weight decreases over successive matings. Sperm competition theory predicts that increased female remating should result in the evolution of larger male testes but smaller ejaculates, and both of these predictions were upheld in seed beetles. Theory also predicts that increased female remating should lead to the evolution of more prudent allocation of ejaculate resources over successive matings. In contrast to this prediction, we found that elevated female remating was associated with a less prudent ejaculate allocation. We suggest that this pattern of correlated evolution, apparently incongruent with classic sperm competition theory, is the result either of trade-offs between ejaculate expenditure and other competing demands or of evolution in total resource acquisition rather than in the evolution of resource allocation.

Keyword
acessory gland products, Callosobruchus, coevolution, mating system, nuptial gift, polyandry, sexual selection, sperm allocation, sperm competition, Zabrotes
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-61565 (URN)10.1111/j.1420-9101.2007.01494.x (DOI)
Available from: 2011-08-23 Created: 2011-08-23 Last updated: 2017-12-08Bibliographically approved
5. Correlated evolution between male and female primary reproductive characters in seed beetles
Open this publication in new window or tab >>Correlated evolution between male and female primary reproductive characters in seed beetles
2011 (English)In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 25, no 3, 634-640 p.Article in journal (Refereed) Published
Abstract [en]

Because males and females of internally inseminating species interact directly during mating, adaptations in one sex in primary reproductive traits may trigger an evolutionary response in the other sex. Divergent postcopulatory sexual selection is considered the main driving force behind the evolution of many male and female reproductive traits, generating unique morphologies and physiologies that can contribute to reproductive isolation and, ultimately, speciation. 2. The focus of most previous studies of the evolution of primary reproductive characters has been male reproductive traits and ejaculate or sperm characteristics. However, in order to more fully understand the evolution of primary reproductive characters it is crucial that we also include female traits. 3. In insects, both the size and the composition of the ejaculate have been shown to influence female reproduction in numerous ways by affecting female remating behaviour, female fecundity and female life span. Here, we employ a phylogenetic comparative approach to assess correlated evolution between primary reproductive characters in males and those in females in a group of seed beetles (Chrysomelidae: Bruchinae). We further explore correlated evolution between ejaculate size and female fitness in these insects. 4. Our analyses revealed positive correlated evolution between three internal female reproductive traits and ejaculate weight as well as correlated evolution between ejaculate weight and female fitness. We discuss the causal factors behind this correlated evolution and suggest that the evolution of larger ejaculates, primarily by postcopulatory sexual selection, causes selection for larger primary sexual traits in females to allow females to more rapidly process ejaculates. This may then feedback on postcopulatory selection in males, reinforcing selection for larger ejaculates. 5. Our results show that the primary reproductive traits of males and females show correlated evolution and suggest that intersexual co-evolution may affect the evolution of female fitness.

Keyword
Bruchinae, Callosobruchus, co-evolution, fitness, genitalia, phylogenetic least squares regression, postcopulatory sexual selection, reproductive traits, sexual selection, sperm competition
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-61551 (URN)10.1111/j.1365-2435.2010.01809.x (DOI)
Available from: 2011-08-23 Created: 2011-08-23 Last updated: 2017-12-08Bibliographically approved

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