Research

One of our main research themes is sexual selection and the evolution of sexual traits and mating behaviour. In brief, we study male allocation of resources to traits associated with mate acquisition and competitive fertilization, the factors underlying male fitness under competitive conditions, and how male and female reproductive traits have changed over evolutionary time in response to sexual selection. We use comparative, experimental and molecular approaches in a range of organisms.

Sexual selection on condition-dependent traits

Due to immediate fitness benefits, males tend to maximize their investment in ornaments or armaments involved in mate acquisition, and in ejaculate size and quality that can influence competitive fertilization success among rival males. However, these traits tend to be energetically costly, so that males with limited resources available are constrained in their investment, thereby having a fitness disadvantage. Several theoretical models predict that the condition-dependent expression of such costly traits allows females to assess the underlying genetic quality of males and gain genetic benefits for their offspring when mating with the highest-quality males (those with the most exaggerated traits). However, a genetic link between trait expression and male genetic quality has rarely been tested, and nearly nothing is known about the level of condition dependence in postmating sexual traits and how it relates to fitness outcomes. Using quantitative genetic crossing designs in Drosophila melanogaster as a model system, we are addressing the following goals:

  • Quantify genetic variation in male and female quality
  • Quantify condition dependence of sexual and non-sexual traits
  • Examine intensity of sexual selection on traits relative to their condition dependence and quantify the indirect fitness consequences

In parallel, using cross-generational experiments, we are testing new theoretical models of sexual selection and condition dependence that are based on non-genetic transmission of male condition effects to the next generation.

Lüpold S, Manier MK, Puniamoorthy N, Schoff C, Starmer WT, Buckley Luepold SH, Belote JM & Pitnick S. 2016. How sexual selection can drive the evolution of costly sperm ornamentation. Nature 533: 535-538.

Lüpold S, Pitnick S, Berben KS, Blengini CS, Belote JM & Manier MK. 2013. Female mediation of competitive fertilization success in Drosophila melanogaster. Proc Natl Acad Sci USA 110: 10693-10698.

Lüpold S, Manier MK, Berben KS, Smith KJ, Daley BD, Buckley SH, Belote JM & Pitnick S. 2012. How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster. Curr Biol 66: 1607-1617.

Glow-in-the-dark sperm of Drosophila melanogaster

Mechanisms underlying postcopulatory sexual selection and reproductive isolation in Drosophila

We are using Drosophila species as model organisms and apply genetic engineering approaches (i.e., fly populations transformed to produce sperm with green or red fluorescently tagged heads) to study the adaptive significance of intraspecific variation in ejaculate traits. This unique research material enables direct visualization of sperm behavior and fate within their selective environment (i.e., the female reproductive tract) while distinguishing between the sperm from competing males (see VIDEO). So far, our research has demonstrated that (1) males adjust their ejaculates depending on the mating status and reproductive quality of the female; (2) multiple ejaculate traits (e.g., sperm length, velocity and number) are under strong genetic control and, collectively, determine competitive fertilization success, with different ejaculate traits being critical at different stages after female remating; and (3) females can influence the outcome of the competition among ejaculates. More recently, we have also explored the adaptive significance and underlying mechanisms of genetic variation in male x male x female interactions.

In parallel, we have extensively investigated the divergence of the processes underlying conspecific sperm precedence and reproductive isolation among sibling species D. simulans and D. mauritiana. Females of these species show significant differences in the way they store and utilize sperm from different males. Importantly, when males of these different species compete for fertilization in the same female (i.e. conspecific and heterospecific mating), females show a clear preference for sperm of their conspecific mate through differential sperm storage and use. Diversifying (allopatric) postcopulatory sexual selection thus seems to quickly result in reproductive isolation. Combined with the detailed intraspecific examination, our results greatly advance our knowledge of the fundamental microevolutionary processes underlying the important macroevolutionary patterns of biodiversity, which are receiving growing attention in studies of sexual selection.

Lüpold S, Manier MK, Puniamoorthy N, Schoff C, Starmer WT, Buckley Luepold SH, Belote JM & Pitnick S. 2016. How sexual selection can drive the evolution of costly sperm ornamentation. Nature 533: 535-538.

Manier MK, Lüpold S, Belote JM, Starmer WT, Berben KS, Ala-Honkola O, Collins WF & Pitnick S. 2013. Postcopulatory sexual selection generates speciation phenotypes in Drosophila. Curr Biol 23: 1853-1862.

Lüpold S, Pitnick S, Berben KS, Blengini CS, Belote JM & Manier MK. 2013. Female mediation of competitive fertilization success in Drosophila melanogaster. Proc Natl Acad Sci USA 110: 10693-10698.

Manier MK, Lüpold S, Pitnick S & Starmer WT. 2013. An analytical framework for estimating fertilization bias and the fertilization set from multiple sperm-storage organs. Am Nat 182:552-561.

Manier MK, Belote JM, Lüpold S, Ala-Honkola O, Berben KS, Collins WF & Pitnick S. 2013. Rapid diversification of sperm precedence traits and processes among three sibling Drosophila species. Evolution 67: 2348-2362.

Lüpold S, Manier MK, Berben KS, Smith KJ, Daley BD, Buckley SH, Belote JM & Pitnick S. 2012. How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster. Curr Biol 66: 1607-1617.

Droge-Young EM, Manier MK, Lüpold S, Belote JM & Pitnick S. 2012. Covariance among premating, post-copulatory and viability fitness components in Drosophila melanogaster and their influence on paternity measurement. J Evol Biol 25: 1555-1563.

Lüpold S, Manier MK, Ala-Honkola O, Belote JM & Pitnick S. 2011. Male Drosophila melanogaster adjust ejaculate size based on female mating status, fecundity, and age. Behav Ecol 22: 184-191.

Sexual selection and sexual dimorphism in Drosophila prolongata

Drosophila prolongata is quite an exception among drosophilid flies, but remains almost entirely unstudied. Not only are males larger than females, but they also have greatly exaggerated forelegs that they use in both male-male contests and to court females. In addition, they show elaborate courtship behaviour, and males can 'steal' females from their rivals (see VIDEO). With these morphological and behavioural characteristics being likely to have evolved under sexual selection, we want to understand their fitness consequences, the selective process underlying their variation or trade-offs with other reproductive traits. To this end, we will use experimental, morphological, physiological and molecular approaches.

Mule deer. Photo credit: Rich Keen / DPRA

Trade-offs among reproductive investments

Whatever resources an individual invests in one trait, it cannot invest in others. Consequently, trade-offs in resource allocation are often predicted. However, comparisons between individuals or species can become more complicated, because some may simply have more resources available to invest overall than others, which can result in positive rather than negative relationships between traits. Similarly, some traits can be positively related and, jointly, trade off against other, possibly unmeasured traits. We are interested in understanding how different, energetically costly traits are associated with one another and how selection shapes these relationships. We are focusing primarily on combinations of reproductive traits, for example sperm number vs. sperm size or premating vs. postmating sexual traits (e.g., male weapons vs. testes), given that males attempt to maximize their investment in all these traits due to their direct fitness benefits.

In recent work using meta-analytical tools, we have shown that the trade-off between sperm size and number depends on the mechanism of postmating sexual selection and the space at the site of fertilization relative to the numbers of sperm competing. Selection in large organisms tends to disproportionately favour sperm number over sperm length, because sperm risk being lost or diluted in the spacious female reproductive tract. Small organisms, with limited space, tend to show a reversed pattern. Transferring more competitive sperm, able to displace rival sperm from storage, appears to be a better strategy than simply increasing sperm quantity and having excess sperm never even reaching storage. Similarly, we have shown how the male's ability to monopolize females changes relative allocation to pre- and postmating sexual traits. Relative to premating weapons, testes become increasingly important as the ability of warding off rival males declines and the risk of sperm competition increases. So, the relationship between pre- and postmating sexual traits can vary between strongly positive and strongly negative.

Simmons LW, Lüpold S & Fitzpatrick JL. 2017. Evolutionary trade-off between secondary sexual traits and ejaculates. Trends Ecol Evol 32: 964-976.

Lüpold S, Jin L & Liao WB. 2017. Population density and structure drive differential investment in pre- and postmating sexual traits in frogs. Evolution 71: 1686-1699.

Lüpold S & Fitzpatrick JL. 2015. Sperm size trumps sperm number in mammalian ejaculate evolution. Proc R Soc B 282: 20152122.

Lüpold S, Simmons LW, Tomkins JL & Fitzpatrick JL. 2015. No evidence for a trade-off between sperm length and male premating weaponry. J Evol Biol 28: 2187-2195.

Fitzpatrick JL & Lüpold S. 2014. Sexual selection and the evolution of ejaculate quality. Mol Human Reprod 20: 1180-1189.

Lüpold S, Tomkins JL, Simmons LW & Fitzpatrick JL. 2014. Female monopolization mediates the relationship between pre- and postcopulatory sexual traits. Nat Commun 5: 3184.

Lüpold S. 2013. Ejaculate quality and constraints in relation to sperm competition levels among eutherian mammals. Evolution 67: 3052-3060.

Immler S, Pitnick S, Parker GA, Durrant KL, Lüpold S, Calhim S & Birkhead TR. 2011. Resolving variation in the reproductive tradeoff between sperm size and number. Proc Natl Acad Sci USA 108: 5325-5330.

Evolution of reproductive traits in birds

Our earlier research also focused on understanding the processes underlying the stunning diversification in sperm morphology and its associations with sperm function in passerine birds. For example, in comparative studies, focusing primarily of New World Blackbirds (Icteridae), we have shown how sperm morphology is shaped through postcopulatory sexual selection, possibly because longer sperm can swim faster (and thus potentially have a fertilization advantage). Associated with this variation in sperm morphology and selection for longer and greater numbers of sperm through sperm competition, we also found adaptations in testicular morphology and spermatogenic efficiency. Importantly, various constraints in sperm production can result in trade-offs between sperm size and number, but the way these trade-offs manifest themselves depends on the conditions at the site of fertilization and the processes of sperm competition.

We have also documented systematic variation in sperm morphology across the species range of the red-winged blackbird (Agelaius phoeniceus). This species exhibits among-population diversity in mating systems, and our results suggest that the sperm diversity may track the expansion of this species from its origin. Finally, although sperm size and shape are typically assumed to be consistent within males, we have shown in the same species that sperm morphology, velocity and quantity can be phenotypically and adaptively plastic across the breeding season.

Fitzpatrick JL & Lüpold S. 2014. Sexual selection and the evolution of ejaculate quality. Mol Human Reprod 20: 1180-1189.

Lüpold S, Birkhead TR, Westneat DF. 2012. Seasonal variation in ejaculate traits of male red-winged blackbirds (Agelaius phoeniceus). Behav Ecol Sociobiol 66: 1607-1617.

Immler S, Pitnick S, Parker GA, Durrant KL, Lüpold S, Calhim S & Birkhead TR. 2011. Resolving variation in the reproductive tradeoff between sperm size and number. Proc Natl Acad Sci USA 108: 5325-5330.

Lüpold S, Wistuba J, Damm OS, Rivers JW & Birkhead TR. 2011. Sperm competition leads to functional adaptations in avian testes to maximize sperm quantity and quality. Reproduction 141: 595-605.

Lüpold S, Westneat DF & Birkhead TR. 2011. Geographical variation in sperm morphology in the redwinged blackbird (Agelaius phoeniceus). Evol Ecol 25: 373-390.

Lüpold S, Calhim S, Immler S & Birkhead, TR. 2009. Sperm morphology and sperm velocity in passerine birds. Proc R Soc Lond B 276: 1175-1181.

Lüpold S, Linz GM & Birkhead TR. 2009. Sperm design and variation in the New World blackbirds (Icteridae). Behav Ecol Sociobiol 63: 899-909.

Lüpold S, Linz GM, Rivers JW, Westneat DF & Birkhead TR. 2009. Sperm competition selects beyond relative testes size in birds. Evolution 63: 391-402.