Publications by authors named "Kirstin S Berben"

7 Publications

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Postcopulatory sexual selection generates speciation phenotypes in Drosophila.

Curr Biol 2013 Oct 26;23(19):1853-62. Epub 2013 Sep 26.

Department of Biology, Syracuse University, Syracuse, NY 13244, USA.

Background: Identifying traits that reproductively isolate species, and the selective forces underlying their divergence, is a central goal of evolutionary biology and speciation research. There is growing recognition that postcopulatory sexual selection, which can drive rapid diversification of interacting ejaculate and female reproductive tract traits that mediate sperm competition, may be an engine of speciation. Conspecific sperm precedence (CSP) is a taxonomically widespread form of reproductive isolation, but the selective causes and divergent traits responsible for CSP are poorly understood.

Results: To test the hypothesis that postcopulatory sexual selection can generate reproductive isolation, we expressed GFP or RFP in sperm heads of recently diverged sister species, Drosophila simulans and D. mauritiana, to enable detailed resolution of species-specific sperm precedence mechanisms. Between-species divergence in sperm competition traits and mechanisms prompted six a priori predictions regarding mechanisms of CSP and degree of cross asymmetry in reproductive isolation. We resolved four distinct mechanisms of CSP that were highly consistent with predictions. These comprise interactions between multiple sex-specific traits, including two independent mechanisms by which females exert sophisticated control over sperm fate to favor the conspecific male.

Conclusions: Our results confirm that reproductive isolation can quickly arise from diversifying (allopatric) postcopulatory sexual selection. This experimental approach to "speciation phenotypes" illustrates how knowledge of sperm precedence mechanisms can be used to predict the mechanisms and extent of reproductive isolation between populations and species.
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http://dx.doi.org/10.1016/j.cub.2013.07.086DOI Listing
October 2013

Inbreeding reveals mode of past selection on male reproductive characters in Drosophila melanogaster.

Ecol Evol 2013 Jul 3;3(7):2089-102. Epub 2013 Jun 3.

Department of Biology, Syracuse University Syracuse, New York ; Department of Biological and Environmental Science, University of Jyväskylä PO Box 35, 40014, Finland.

Directional dominance is a prerequisite of inbreeding depression. Directionality arises when selection drives alleles that increase fitness to fixation and eliminates dominant deleterious alleles, while deleterious recessives are hidden from it and maintained at low frequencies. Traits under directional selection (i.e., fitness traits) are expected to show directional dominance and therefore an increased susceptibility to inbreeding depression. In contrast, traits under stabilizing selection or weakly linked to fitness are predicted to exhibit little-to-no inbreeding depression. Here, we quantify the extent of inbreeding depression in a range of male reproductive characters and then infer the mode of past selection on them. The use of transgenic populations of Drosophila melanogaster with red or green fluorescent-tagged sperm heads permitted in vivo discrimination of sperm from competing males and quantification of characteristics of ejaculate composition, performance, and fate. We found that male attractiveness (mating latency) and competitive fertilization success (P2) both show some inbreeding depression, suggesting they may have been under directional selection, whereas sperm length showed no inbreeding depression suggesting a history of stabilizing selection. However, despite having measured several sperm quality and quantity traits, our data did not allow us to discern the mechanism underlying the lowered competitive fertilization success of inbred (f = 0.50) males.
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http://dx.doi.org/10.1002/ece3.625DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3728949PMC
July 2013

Rapid diversification of sperm precedence traits and processes among three sibling Drosophila species.

Evolution 2013 Aug 29;67(8):2348-62. Epub 2013 May 29.

Department of Biology, Syracuse University, Syracuse, New York 13244, USA.

Postcopulatory sexual selection is credited with driving rapid evolutionary diversification of reproductive traits and the formation of reproductive isolating barriers between species. This judgment, however, has largely been inferred rather than demonstrated due to general lack of knowledge about processes and traits underlying variation in competitive fertilization success. Here, we resolved processes determining sperm fate in twice-mated females, using transgenic Drosophila simulans and Drosophila mauritiana populations with fluorescently labeled sperm heads. Comparisons among these two species and Drosophila melanogaster revealed a shared motif in the mechanisms of sperm precedence, with postcopulatory sexual selection potentially occurring during any of the three discrete stages: (1) insemination; (2) sperm storage; and (3) sperm use for fertilization, and involving four distinct phenomena: (1) sperm transfer; (2) sperm displacement; (3) sperm ejection; and (4) sperm selection for fertilizations. Yet, underlying the qualitative similarities were significant quantitative differences in nearly every relevant character and process. We evaluate these species differences in light of concurrent investigations of within-population variation in competitive fertilization success and postmating/prezygotic reproductive isolation in hybrid matings between species to forge an understanding of the relationship between microevolutionary processes and macroevolutionary patterns as pertains to postcopulatory sexual selection in this group.
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http://dx.doi.org/10.1111/evo.12117DOI Listing
August 2013

Female mediation of competitive fertilization success in Drosophila melanogaster.

Proc Natl Acad Sci U S A 2013 Jun 11;110(26):10693-8. Epub 2013 Jun 11.

Department of Biology, Syracuse University, Syracuse, NY 13244, USA.

How females store and use sperm after remating can generate postcopulatory sexual selection on male ejaculate traits. Variation in ejaculate performance traits generally is thought to be intrinsic to males but is likely to interact with the environment in which sperm compete (e.g., the female reproductive tract). Our understanding of female contributions to competitive fertilization success is limited, however, in part because of the challenges involved in observing events within the reproductive tract of internally fertilizing species while discriminating among sperm from competing males. Here, we used females from crosses among isogenic lines of Drosophila melanogaster, each mated to two genetically standardized males (the first with green- and the second with red-tagged sperm heads) to demonstrate heritable variation in female remating interval, progeny production rate, sperm-storage organ morphology, and a number of sperm performance, storage, and handling traits. We then used multivariate analyses to examine relationships between this female-mediated variation and competitive paternity. In particular, the timing of female ejection of excess second-male and displaced first-male sperm was genetically variable and, by terminating the process of sperm displacement, significantly influenced the relative numbers of sperm from each male competing for fertilization, and consequently biased paternity. Our results demonstrate that females do not simply provide a static arena for sperm competition but rather play an active and pivotal role in postcopulatory processes. Resolving the adaptive significance of genetic variation in female-mediated mechanisms of sperm handling is critical for understanding sexual selection, sexual conflict, and the coevolution of male and female reproductive traits.
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http://dx.doi.org/10.1073/pnas.1300954110DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3696778PMC
June 2013

How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster.

Curr Biol 2012 Sep 26;22(18):1667-72. Epub 2012 Jul 26.

Department of Biology, Syracuse University, Syracuse, NY 13244-1270, USA.

Success in sperm competition, occurring whenever females mate with multiple males, is predicted to be influenced by variation in ejaculate quality and interactions among competing sperm. Yet, apart from sperm number, relevant ejaculate characteristics and sperm-sperm interactions are poorly understood, particularly within a multivariate framework and the natural selective environment of the female reproductive tract. Here, we used isogenic lines of Drosophila melanogaster with distinguishable sperm to demonstrate and partition genetic variation in multiple sperm quality and performance traits. Next, by competing males from different lines, we show how rival sperm significantly influence each other's velocity and reveal that males with relatively slow and/or long sperm better displace rival sperm and resist displacement, thus avoiding ejection by the female from her reproductive tract. Finally, we establish fitness consequences of genetic variation in sperm quality and its role in securing a numerical advantage in storage by showing that offspring paternity is determined strictly by the representation of stored, competing sperm. These results provide novel insight into complex postcopulatory processes, illustrate that different ejaculate traits are critical at different biologically relevant time-points, and provide a critical foundation for elucidating the role of postcopulatory sexual selection in trait diversification and speciation.
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http://dx.doi.org/10.1016/j.cub.2012.06.059DOI Listing
September 2012

Resolving mechanisms of competitive fertilization success in Drosophila melanogaster.

Science 2010 Apr 18;328(5976):354-7. Epub 2010 Mar 18.

Department of Biology, Syracuse University, Syracuse, NY 13244-1270, USA.

Our understanding of postcopulatory sexual selection has been constrained by an inability to discriminate competing sperm of different males, coupled with challenges of directly observing live sperm inside the female reproductive tract. Real-time and spatiotemporal analyses of sperm movement, storage, and use within female Drosophila melanogaster inseminated by two transgenic males with, respectively, green and red sperm heads allowed us to unambiguously discriminate among hypothesized mechanisms underlying sperm precedence, including physical displacement and incapacitation of "resident" sperm by second males, female ejection of sperm, and biased use of competing sperm for fertilization. We find that competitive male fertilization success derives from a multivariate process involving ejaculate-female and ejaculate-ejaculate interactions, as well as complex sperm behavior in vivo.
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http://dx.doi.org/10.1126/science.1187096DOI Listing
April 2010

Size-dependent alternative male mating tactics in the yellow dung fly, Scathophaga stercoraria.

Proc Biol Sci 2009 Sep 24;276(1671):3229-37. Epub 2009 Jun 24.

Department of Biology, Syracuse University, Syracuse, NY 13244-1270, USA.

Whenever males can monopolize females and/or resources used by females, the opportunity for sexual selection will be great. The greater the variation among males in reproductive success, the greater the intensity of selection on less competitive males to gain matings through alternative tactics. In the yellow dung fly, Scathophaga stercoraria, males aggressively compete for access to receptive, gravid females on fresh dung. Larger males are better able to acquire mates and to complete copulation successfully and guard the female throughout oviposition. Here we demonstrate that when an alternative resource is present where females aggregate (i.e. apple pomace, where both sexes come to feed), smaller males will redirect their searching for females from dung to the new substrate. In addition, we identify a class of particularly small males on the alternative substrate that appears never to be present searching for females on or around dung. Smaller males were found to have a mating 'advantage' on pomace, in striking contrast to the pattern observed on dung, providing further support for the existence of an alternative male reproductive tactic in this species.
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http://dx.doi.org/10.1098/rspb.2009.0632DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2817166PMC
September 2009
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