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Featured researches published by Mollie K. Manier.


Science | 2010

Resolving Mechanisms of Competitive Fertilization Success in Drosophila melanogaster

Mollie K. Manier; John M. Belote; Kirstin S. Berben; David Novikov; Will T. Stuart; Scott Pitnick

Battle of the Sperm In insects, sperm from multiple matings are stored and retained, and are thought to compete for ova within a females reproductive tract. Manier et al. (p. 354, published online 18 March) visualized sperm from fruit flies transgenically tagged with green or red fluorescent protein within the reproductive tracts of female flies. Sperm showed more mobility within the female storage organs than expected, with those from the most recent copulation displacing sperm from previous males; however, sperm viability remained consistent over long-term storage and each males sperm was equally competitive in fertilizing the females eggs. Fluorescently labeled sperm allow direct visualization of their activity within the female reproductive tract of flies. 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.


Current Biology | 2012

How Multivariate Ejaculate Traits Determine Competitive Fertilization Success in Drosophila melanogaster

Stefan Lüpold; Mollie K. Manier; Kirstin S. Berben; Kyle J. Smith; Bryan D. Daley; Shannon H. Buckley; John M. Belote; Scott Pitnick

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 others 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.


Proceedings of the National Academy of Sciences of the United States of America | 2013

Female mediation of competitive fertilization success in Drosophila melanogaster

Stefan Lüpold; Scott Pitnick; Kirstin S. Berben; Cecilia S. Blengini; John M. Belote; Mollie K. Manier

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.


Proceedings of the Royal Society of London B: Biological Sciences | 2006

Ecological correlates of population genetic structure: a comparative approach using a vertebrate metacommunity

Mollie K. Manier; Stevan J. Arnold

Identifying ecological factors associated with population genetic differentiation is important for understanding microevolutionary processes and guiding the management of threatened populations. We identified ecological correlates of several population genetic parameters for three interacting species (two garter snakes and an anuran) that occupy a common landscape. Using multiple regression analysis, we found that species interactions were more important in explaining variation in population genetic parameters than habitat and nearest-neighbour characteristics. Effective population size was best explained by census size, while migration was associated with differences in species abundance. In contrast, genetic distance was poorly explained by the ecological correlates that we tested, but geographical distance was prominent in models for all species. We found substantially different population dynamics for the prey species relative to the two predators, characterized by larger effective sizes, lower gene flow and a state of migration-drift equilibrium. We also identified an escarpment formed by a series of block faults that serves as a barrier to dispersal for the predators. Our results suggest that successful landscape-level management should incorporate genetic and ecological data for all relevant species, because even closely associated species can exhibit very different population genetic dynamics on the same landscape.


Sperm Biology#R##N#An Evolutionary Perspective | 2009

9 – Sperm and speciation

Daniel J. Howard; Stephen R. Palumbi; Leanna M. Birge; Mollie K. Manier

Publisher Summary There is general recognition among evolutionists that no matter how one defines a species, the boundaries between distinct, sexually reproducing species are maintained by barriers to gene flow at individual loci. Isolating barriers have typically been categorized into those operating before fertilization (prezygotic) and after fertilization (postzygotic). Prezygotic reproductive barriers can arise due to the evolution of habitat utilization differences, mating behavior differences, and/or phenological differences between incipient species. Postzygotic isolating barriers encompass hybrid inviability, hybrid sterility and hybrid breakdown. This chapter is concerned with the set of prezygotic barriers that occur in closely related animal species after ejaculation or spawning and before fertilization, resulting in postmating, prezygotic (PMPZ) isolation. The transfer or spawning of sperm sets the stage for the operation of PMPZ barriers to gene exchange. The environment of the female reproductive tract eliminates or kills many male gametes, even conspecific ones, in a variety of ways. These barriers to fertilization by conspecific sperm may also serve as barriers to fertilization by heterospecific sperm. Moreover, in heterospecific pairings, sperm may fail to move appropriately in the female reproductive tract. The importance of chemotaxis in mediating PMPZ isolation varies among major taxonomic groups and appears to be related to whether fertilization occurs internally or externally. In insects, the proteins in the seminal fluid can influence the fertilization process in a number of ways including: the storage and capacitation of sperm; the induction of peristalsis in the female reproductive tract; and the induction of ovulation.


Evolution | 2013

Rapid Diversification Of Sperm Precedence Traits And Processes Among Three Sibling Drosophila Species

Mollie K. Manier; John M. Belote; Kirstin S. Berben; Stefan Lüpold; Outi Ala-Honkola; William F. Collins; Scott Pitnick

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.


Trends in Ecology and Evolution | 2017

Postmating Female Control: 20 Years of Cryptic Female Choice

Renée C. Firman; Clelia Gasparini; Mollie K. Manier; Tommaso Pizzari

Cryptic female choice (CFC) represents postmating intersexual selection arising from female-driven mechanisms at or after mating that bias sperm use and impact male paternity share. Although biologists began to study CFC relatively late, largely spurred by Eberhard’s book published 20 years ago, the field has grown rapidly since then. Here, we review empirical progress to show that numerous female processes offer potential for CFC, from mating through to fertilization, although seldom has CFC been clearly demonstrated. We then evaluate functional implications, and argue that, under some conditions, CFC might have repercussions for female fitness, sexual conflict, and intersexual coevolution, with ramifications for related evolutionary phenomena, such as speciation. We conclude by identifying directions for future research in this rapidly growing field.


Genome Biology and Evolution | 2010

Whole-Genome Positive Selection and Habitat-Driven Evolution in a Shallow and a Deep-Sea Urchin

Thomas A. Oliver; David A. Garfield; Mollie K. Manier; Ralph Haygood; Gregory A. Wray; Stephen R. Palumbi

Comparisons of genomic sequence between divergent species can provide insight into the action of natural selection across many distinct classes of proteins. Here, we examine the extent of positive selection as a function of tissue-specific and stage-specific gene expression in two closely-related sea urchins, the shallow-water Strongylocentrotus purpuratus and the deep-sea Allocentrotus fragilis, which have diverged greatly in their adult but not larval habitats. Genes that are expressed specifically in adult somatic tissue have significantly higher dN/dS ratios than the genome-wide average, whereas those in larvae are indistinguishable from the genome-wide average. Testis-specific genes have the highest dN/dS values, whereas ovary-specific have the lowest. Branch-site models involving the outgroup S. franciscanus indicate greater selection (ωFG) along the A. fragilis branch than along the S. purpuratus branch. The A. fragilis branch also shows a higher proportion of genes under positive selection, including those involved in skeletal development, endocytosis, and sulfur metabolism. Both lineages are approximately equal in enrichment for positive selection of genes involved in immunity, development, and cell–cell communication. The branch-site models further suggest that adult-specific genes have experienced greater positive selection than those expressed in larvae and that ovary-specific genes are more conserved (i.e., experienced greater negative selection) than those expressed specifically in adult somatic tissues and testis. Our results chart the patterns of protein change that have occurred after habitat divergence in these two species and show that the developmental or functional context in which a gene acts can play an important role in how divergent species adapt to new environments.


Nature | 2016

How sexual selection can drive the evolution of costly sperm ornamentation.

Stefan Lüpold; Mollie K. Manier; Nalini Puniamoorthy; Christopher Schoff; William T. Starmer; Shannon H. Buckley Luepold; John M. Belote; Scott Pitnick

Post-copulatory sexual selection (PSS), fuelled by female promiscuity, is credited with the rapid evolution of sperm quality traits across diverse taxa. Yet, our understanding of the adaptive significance of sperm ornaments and the cryptic female preferences driving their evolution is extremely limited. Here we review the evolutionary allometry of exaggerated sexual traits (for example, antlers, horns, tail feathers, mandibles and dewlaps), show that the giant sperm of some Drosophila species are possibly the most extreme ornaments in all of nature and demonstrate how their existence challenges theories explaining the intensity of sexual selection, mating-system evolution and the fundamental nature of sex differences. We also combine quantitative genetic analyses of interacting sex-specific traits in D. melanogaster with comparative analyses of the condition dependence of male and female reproductive potential across species with varying ornament size to reveal complex dynamics that may underlie sperm-length evolution. Our results suggest that producing few gigantic sperm evolved by (1) Fisherian runaway selection mediated by genetic correlations between sperm length, the female preference for long sperm and female mating frequency, and (2) longer sperm increasing the indirect benefits to females. Our results also suggest that the developmental integration of sperm quality and quantity renders post-copulatory sexual selection on ejaculates unlikely to treat male–male competition and female choice as discrete processes.


The American Naturalist | 2013

An Analytical Framework for Estimating Fertilization Bias and the Fertilization Set from Multiple Sperm-Storage Organs

Mollie K. Manier; Stefan Lüpold; Scott Pitnick; William T. Starmer

How sperm from competing males are used to fertilize eggs is poorly understood yet has important implications for postcopulatory sexual selection. Sperm may be used in direct proportion to their numerical representation within the fertilization set or with a bias toward one male over another. Previous theoretical treatments have assumed a single sperm-storage organ, but many taxa possess multiple organs or store sperm within multiple regions of the reproductive tract. In Drosophila, females store sperm in two distinct storage organ types: the seminal receptacle (SR) and the paired spermathecae. Here, we expand previous “raffle” models to describe “fertilization bias” independently for sperm within the SR and the spermathecae and estimate the fertilization set based on the relative contribution of sperm from the different sperm-storage organ types. We apply this model to three closely related species to reveal rapid divergence in the fertilization set and the potential for female sperm choice.

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