Areas of Expertise
Evolutionary genetics, molecular genetics, molecular evolution, sexual selection, behavioral ecology, spermatogenesis, development, epigenetics, genomics, bioinformatics, Drosophila
As an organismal biologist, my curiosity comes in two flavors: how and why. The how addresses proximal questions of cellular, molecular, and developmental mechanisms. For example, how do insect sperm remain motile for days to years within the female reproductive tract? The why addresses larger evolutionary questions, such as why do certain traits evolve rapidly? I have broad interests that encompass microevolution (processes acting within species), macroevolution (diversification among species and higher order lineages), molecular and cellular mechanisms of phenotypic diversity, and systems biology. My research program spans diverse fields, but it is unified by a common goal of understanding the how and the why of complex phenotypes important for fitness. At present, we are using a wide range of approaches, from phylogenetic to molecular in scale, to explore questions along three axes: 1) structure and function of giant sperm and sperm storage organs, 2) transgenerational effects of parental environment on offspring phenotype, and 3) molecular mechanisms of communication along the microbiota-gut-brain axis.
Reproductive traits have long fascinated evolutionary biologists because they are important in ensuring fitness, they tend to evolve rapidly, and they can play large roles in reproductive isolation.
Sperm are especially interesting, because they are the most morphologically variable cell type in multicellular animals (Metazoa). In addition, they are unique among metazoan cells in being cast forth into a foreign environment to function as free-living organisms until fertilization. As a result, they are often subject to species-specific selective pressures that drive their rapid evolution and extraordinary diversification, often resulting in truly bizarre forms (Fig. 1).
Selective forces driving sperm evolution include sperm competition and interactions with the female environment (in internal fertilizers). Indeed, female sperm storage organs can be just as diverse as sperm traits and in ways that suggest male-female co-evolution (Fig. 2).
My research explores the mechanistic causes and evolutionary consequences of adaptive variation in sperm and sperm storage organs. To this end, I use comparisons among closely related species, behavioral ecology experiments, genotype-phenotype mapping, and cell culture approaches in Drosophila.
Our research questions include:
- How does sperm competition work?
- What are mechanisms of conspecific precedence between closely related species?
- What are the functional relationships among post-copulatory events influencing paternity success?
- What are the roles of males, females and male x female interactions in determining paternity success?
- How does male condition influence paternity success?
- What genes control sperm length and sperm storage organ length?
- How do these genes control morphogenesis?
B.A., University of California, Berkeley, 1997
Ph.D., Oregon State University, 2005
NIH NRSA Postdoctoral Fellow, Hopkins Marine Station of Stanford University, 2005-2008
Postdoctoral Researcher, Syracuse University, 2008-2013
Manier MK, G Welch, C Van Nispen, M Bakst, and J Long. Low mobility sperm phenotype in the turkey: impact on sperm morphometrics and early embryonic death. Reproduction in Domestic Animals in press.
Firman R, C Gasparini, MK Manier, and T Pizzari. 2017. Postmating control: 20 years of studying cryptic female choice. Trends in Ecology and Evolution 32: 368-382. (doi: 10.1016/j.tree.2017.02.010).
Firman R, C Gasparini, MK Manier, and T Pizzari. 2017. Reply to Eberhard. Cryptic female choice: a general phenomenon. Trends in Ecology and Evolution 32: 807-808. (doi: 10.1016/j.tree.2017.08.010).
Zajitschek F, S Zajitschek and MK Manier. 2017. High-protein paternal diet confers an advantage to sons in sperm competition. Biology Letters 13: 20160914 (doi: 10.1098/rsbl.2016.0914). Correction to ‘High-protein paternal diet confers an advantage to sons in sperm competition’. https://doi.org/10.1098/rsbl.2017.0297.
Elgin SCR, C Hauser, TM Holzen, C Jones, A Kleinschmit, J Leatherman and Genomics Education Partnership. 2017. The GEP: Crowd-sourcing big data analysis with undergraduates. Trends in Genetics 33: 81-85 (doi: 10.1016/j.tig.2016.11.004).
Lüpold S, MK Manier, N Puniamoorthy, C Schoff, WT Starmer, SH Buckley Luepold, JM Belote and S Pitnick. 2016. How sexual selection can drive the evolution of costly sperm ornamentation. Nature 533: 535-538 (doi: 10.1038/nature18005).
Ala-Honkola O and MK Manier. 2016. Multiple mechanisms of cryptic female choice act on intraspecific male variation in Drosophila simulans. Behavioral Ecology and Sociobiology 70: 519-532 (doi: 10.1007/s00265-016-2069-3).
Ala-Honkola O., M. K. Manier, S. Lüpold, E. M. Droge-Young, W. F. Collins, J. M. Belote and S. Pitnick. 2014. No inbreeding depression in sperm storage ability or offspring viability in Drosophila melanogaster females. Journal of Insect Physiology 60: 1-6 (doi: 10.1016/j.jinsphys.2013.10.005).
Gress B. E., R. J. Waltzer, S. Lüpold, E. M. Droge-Young, M. K. Manier and S. Pitnick. 2014. Alternative mating tactics in the yellow dung fly: resolving the mechanisms of small male advantage off pasture. Proceedings of the Royal Society London B 281: 2164 (doi: 10.1098/rspb.2013.2164).
Manier, M. K., J. M. Belote, W. T. Starmer, K. S. Berben, S. Lüpold, O. Ala-Honkola, W. F. Collins and S. Pitnick. 2013. Postcopulatory sexual selection generates speciation phenotypes in Drosophila. Current Biology 23: 1853-1862 (doi: 10.1016/j.cub.2013.07.086).
Manier, M. K., S. Lüpold, S. Pitnick, W. T. Starmer. 2013. An analytical framework for estimating fertilization bias from multiple sperm storage organs. American Naturalist 182: 552-561 (doi: 10.1086/671782).
Ala-Honkola, O., D. J. Hosken, M. K. Manier, S. Lüpold, E. M. Droge-Young, K. S. Berben, W. F. Collins, J. M. Belote and S. Pitnick. 2013. Inbreeding reveals mode of past selection on male reproductive characters in Drosophila melanogaster. Ecology and Evolution 3: 2089-2102 (doi: 10.1002/ece3.625).
Manier, M. K., J. M. Belote, S. Lüpold, K. S. Berben, O. Ala-Honkola, W. F. Collins and S. Pitnick. 2013. Rapid diversification of sperm precedence traits and processes among three sibling Drosophila species. Evolution 67: 2348-2362 (doi: 10.1111/evo.12117).
Lüpold, S., S. Pitnick, K. S. Berben, C. S. Blengini, J. M. Belote and M. K. Manier. 2013. Female mediation of competitive fertilization success in Drosophila melanogaster. Proceedings of the National Academy of Sciences 110: 10693-10698 (doi: 10.1073/pnas.1300954110).
Belote, J. M., S. Lüpold, M. K. Manier and S. Pitnick. 2013. Opening a window onto sperm competition. Molecular Reproduction and Development 80: 79 (doi: 10.1002/mrd.22155).
Lüpold, S, M. K. Manier, K. S. Berben, K. J. Smith, B. D. Daly, S. H. Buckley, J. M. Belote and S. Pitnick. 2012. How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster. Current Biology 22: 1667-1672 (doi: 10.1016/j.cub.2012.06.059).
Droge-Young, E. M., M. K. Manier, S. Lüpold, J. M. Belote and S. Pitnick. 2012. Covariance among premating, postcopulatory and viability fitness components in Drosophila melanogaster and their influence on paternity measurement. Journal of Evolutionary Biology 25: 1555-1563 (doi: 10.1111/j.1420-9101.2012.02540.x).
Pespeni, M. H., D. A. Garfield, M. K. Manier and S. R. Palumbi. 2012. Genome-wide polymorphisms show unexpected targets of natural selection. Proceedings of the Royal Society of London B 279: 1412-1420 (doi: 10.1098/rspb.2011.1823).
Ala-Honkola, O., M. K. Manier, S. Lüpold and S. Pitnick. 2011. No evidence for postcopulatory inbreeding avoidance in Drosophila melanogaster. Evolution 65: 2699-2705 (doi:10.1111/j.1558-5646.2011.01317.x).
Lüpold, S., M. K. Manier, O. Ala-Honkola, J. M. Belote, S. Pitnick. 2011. Male Drosophila melanogaster adjust ejaculate size based on female mating status, fecundity and age. Behavioral Ecology 122: 184-191 (doi: 10.1093/beheco/arq193).
Manier, M. K., J. M. Belote, K. S. Berben, D. Novikov, W. T. Stuart and S. Pitnick. 2010. Resolving mechanisms of competitive fertilization success in Drosophila melanogaster. Science 328: 354-357 (doi: 10.1126/science.1187096).
Oliver, T. A., D. A. Garfield, M. K. Manier, R. Haygood, G. A. Wray and S. R. Palumbi. 2010. Whole-genome positive selection and habitat-driven evolution in a shallow and deep-sea urchin. Genome Biology and Evolution 2: 800-814 (doi: 10.1093/gbe/evq063).
Pespeni, M. H., T. A. Oliver, M. K. Manier and S. R. Palumbi. 2010. Restriction Site Tiling Analysis: Accurate discovery and quantitative genotyping of genome-wide polymorphisms using nucleotide arrays. Genome Biology 11: R44 (doi: 10.1186/gb-2010-11-4-r44).
Pitnick, S., K. R. H. Henn, S. Maheaux, D. M. Higginson, J. L. Hurtado-Gonzales, M. K. Manier, K. S. Berben, C. Guptill and J. A. C. Uy. 2009. Size-dependent alternative male mating tactics in the yellow dung fly, Scathophaga stercoraria. Proceedings of the Royal Society of London B 276: 3229-3237 (doi: 10.1098/rspb.2009.0632).
Howard, D., S. R. Palumbi, L. Birge and M. K. Manier. 2009. Sperm and speciation. Pp. 367-403 In Sperm Biology: An Evolutionary Perspective (TR Birkhead, DJ Hosken and S. Pitnick, eds.). Elsevier. Burlington, MA .
Manier, M. K. and S. R. Palumbi. 2008. Intraspecific divergence in sperm morphology of the green sea urchin, Strongylocentrotus droebachiensis: implications for selection in broadcast spawners. BMC Evolutionary Biology 8: 283 (doi: 10.1186/1471-2148-8-283).
Manier, M. K., C. M. Seylor and S. J. Arnold. 2007. Adaptive divergence between ecotypes of the terrestrial garter snake, Thamnophis elegans, assessed with FST-QST comparisons. Journal of Evolutionary Biology 20: 1705-1719 (doi: 10.1111/j.1420-9101.2007.01401.x).
Manier, M. K. and S. J. Arnold. 2006. Ecological correlates of population genetic structure: a comparative approach using a vertebrate metacommunity. Proceedings of the Royal Society, London B 273: 3001-3009 (10.1098/rspb.2006.3678).
Manier M. K. and S. J. Arnold. 2005. Population genetic analysis identifies source-sink dynamics for two sympatric garter snake species (Thamnophis elegans and T. sirtalis). Molecular Ecology 14: 3965-3976 (doi: 10.1111/j.1365-294X.2005.02734.x).
Manier M. K. 2004. Geographic variation in the long-nosed snake (Rhinocheilus lecontei): beyond the subspecies debate. Biological Journal of the Linnean Society 83: 65-85 (doi: 10.1111/j.1095-8312.2004.00373.x).