Fall 2011 - the Department of Biology - Syracuse University

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GRADUATE STUDENT PROFILE:Dawn HigginsonI’ve learned to be vague when strangers ask me what I do. A bluntreply of “I study sperm” typically results in a stunned or mildlybemused expression and a quietly uttered response of “Oh!” Thatends most conversations with non-biologists.Sperm were discovered in 1677 byAntonie van Leeuwenhoek, a draper byprofession and an amateur microscopist.In his spare time, he built simple, singlelens microscopes that could magnifyobjects up to 270x, sufficient to seeeven some bacteria. In his letter to theRoyal Society of London describing hisremarkable discovery, he communicatedthe sensitivity of the topic:“And if your Lordship should considerthat these observations may disgust orscandalize the learned, I earnestly begyour Lordship to regard them as privateand to publish or destroy them as yourLordship see fit.”Fortunately, Leeuwenhoek’s workwas published and attracted considerableattention from scientists at the time.However, the role of sperm and eggs inthe production of new individuals was notunderstood or widely accepted until the1880s. Today, it is common knowledge thattransfer of paternal DNA through spermto an unfertilized egg occurs in all sexuallyreproducing animals.I first became interested in spermwhile working on the evolution ofinsecticide resistance in the pinkbollworm, a pest in cotton fieldsworldwide. The pink bollworm is a smallmoth whose caterpillars eat the developingseed heads from which cotton fiber isharvested. In the United States, pinkbollworm damage is limited by plantingtransgenic cotton plants, geneticallymodified to produce Bt-toxin protein,the gene for which was isolated fromthe bacterium Bacillus thuringiensis. Bttoxinbinds to the gut of caterpillars; thecaterpillars stop feeding and eventuallydie. Outside of legally required “refuges”in which unmodified cotton is planted,virtually all cotton grown currently istransgenic, potentially resulting in intenseselection for bollworms resistant to Bttoxin.After the widespread introductionof Bt cotton to the US agricultural system,the proportion of pink bollworms inArizona fields resistant to Bt-toxin actuallydropped from a surprisingly high level atthe time of introduction to undetectablelevels. As part of a master’s thesis, Iwas tasked with understanding whyresistance to Bt-cotton was not found inthe field despite the ease of generatingresistant pink bollworm strains in the lab.Experiments conducted by members ofmy research group at the University ofArizona revealed that resistant moths wereless likely to survive the winter than mothssusceptible to Bt. Additionally, I foundthat resistant males sired fewer offspringthan susceptible males when competingto fertilize a female’s eggs, despite havingsimilar mating frequencies and fertility.While trying to understand this result, Ilearned that moths and butterflies producetwo types of sperm: one type participatesin fertilization while the second typecontains no DNA. Sperm lacking DNAoften makeup more than 90 percent ofthe total sperm transferred to females. Iwas completely stunned by this fact. Whyspend so much energy making spermthat couldn’t fulfill the primary function offertilization? Follow-up research by my labgroup found that resistant males transferfewer sperm, of both types, to femalesthan do males susceptible to Bt-cotton.After finishing my M.S. degree at theUniversity of Arizona and a brief hiatusworking in a University of Montana labstudying bark beetles (the scourge ofwestern forests, killing whole stands oftrees and increasing the likelihood oflarge-scale wildfires), I still couldn’t stopthinking about the bizarre infertile spermof moths. I found myself borrowing allthe sperm-related books from the libraryand decided that I wanted to investigatethe evolution of unusual sperm traits in adepth that only a Ph.D. dissertation wouldallow. I started looking at grad schools andfound the best place in North America,and arguably the world, to pursue mystudies was in the lab of Scott Pitnickin the Department of Biology at SU. Iapplied, was accepted, and spent the nextseveral years happily submerged in thestudy of how reproductive traits are shapedby selection resulting from male-malecompetition for mates and female choiceof sires.My doctoral research focused onunderstanding why sperm that share acommon function, fertilization, have suchdiverse morphology. For example, withininsects alone, any one of the four mainconstituents of sperm—the acrosome,nucleus, mitochondria or flagellum—maybe absent or form the most prominentfeature of sperm morphology. The answeris, in part, that sperm do much more thanjust fertilize an egg. In the case of specieswith internal fertilization (most terrestrialand some aquatic animals), sperm mustnavigate the often complex chemicaland physical environment of the femalereproductive tract to locate and fuse withan egg. Sperm also often undergo thefinal stages of maturation outside of thebody of the male that produced them. Inaddition,Hisperm typically have to competewith the sperm of rival males within thefemale while avoiding competition withsibling sperm. The diverse morphology ofsperm is believed to reflect adaptations toovercome e these many challenges facingsperm.To test ideas about how spermmorphology ogy evolves, I have focused ondiving beetles es (Dytiscidae). The grouphas been around since the time of thedinosaurs, and today there are nearly4,000 living species. Diving beetlescan be found in almost any lake, pond,stream, or puddle worldwide. Prior to mywork, the sperm of a handful of closelyrelated species had been examined.From this limited sample, it was evidentthat the sperm of diving beetles oftenjoin together at the head to form amulti-sperm conjugate that swims in a14THE DEPARTMENT OF BIOLOGY AT SYRACUSE UNIVERSITY
Figure 1: Sperm pairing in Graphoderusliberus. The heads of two sperm are tightlyjoined (upper left) with the flagella free.coordinated manner before dissociatingprior to fertilization. To determine if suchconjugates are typical for diving beetles, Icharacterized the sperm fromFigure 2: An aggregate composed of six spermapproximately 140 additional species in Rhantus consimilis. The sperm have beendistributed across the family. From this DNA-stained making the heads prominentwork, it was evident that most species (lower left). Aggregates are composed ofproduce conjugates and that amongvariable numbers of sperm within males.species, conjugates take one of threeFigure 3: Dimorphic sperm and a conjugateforms: 1) aggregates, where variableof Hygrotus sayi. Males produce sperm withnumbers of sperm align with their heads this work it is evident that sperm evolvecheckmark-shaped and filamentous headsin register; 2) pairs, where strictly two rapidly but diversification is constrained to(top panel). The tip of one checkmarkshapedhead slips into a pocket at the basesperm join with their heads aligned; 3) particular traits.rouleaux, where the tip of one sperm head Why should diving beetles evolveof another to form orderly stacks calledslips into a pocket at the base of another conjugates to begin with? For divingrouleaux to which filamentous spermto form an orderly stack of sperm (a novel beetles, like other internally fertilizingheads attach (lower panel). The conjugatestype of conjugate unknown prior to my species, the female reproductive tractare composed of hundreds of sperm andresearch). Additionally, males of some is the selective environment of sperm.are highly motile. Sperm have been DNAspecies produce two distinct types of I hypothesized that conjugates mightstained and imaged using epifluorescence.sperm that differ in total length or head allow sperm to maintain positions in theFlagella are not visible.shape. Unlike moths and butterflies, both female close to where eggs are released,sperm morphs contain DNA althoughit is unknown if both can participate infertilization. Formation of conjugates anddimorphism sometimes co-occur, resultingin complex conjugates composed of bothtypes of sperm.I mapped sperm traits ontophylogenetic trees based on DNAand thereby increase their probability ofbeing used for fertilization. If this weretrue, formation of conjugates and aspectsof the female reproductive tract would beexpected to evolve in a correlated manner.Diving beetles have a conduit-stylereproductive tract: sperm enter and travelto the site of storage before exiting throughapparently anchoring within the duct.The few people who aren’t deterredby my response “I study sperm” often askme what is the point of my research andhow does it help humans. I sometimesbristle at this question. Is there nointrinsic value to understanding thegginsonsequence from two mitochondrial and a separate duct to the site of fertilization. origins of the tremendous diversity lifetwo nuclear genes, which representI measured the dimensions of the entrythis planet and how diversity of formsevolutionary relationships between species.duct, storage organ(s) and exit duct of 42affect function their environment?Next, I evaluated how well differentspecies of diving beetles. Using statisticalBut I know this is insufficient. Insteadmodels of sperm evolution fit the observedmethods that control for similarityI explain that despite the discovery ofdistribution of sperm traits the trees.produced by shared evolutionary history, Isperm more than 300 years ago, spermOnce I found the most likely model offound that presence of sperm conjugatesmotility (critically important for fertilityevolution, on, I used this model to infer whatwas correlated with small sperm storagehumans and many other species), thethe sperm of long extinct species of divingorgans and short exit ducts. Furthermore,impact of morphology sperm function,beetles might have looked like. I concludeddimensions of the female reproductiveand the process of fertilization are poorlyaggregates are the ancestral sperm form tract t changed advance of spermunderstood. As with many mammals,diving beetles and subsequently diversifiedconjugation, indicating that sperm evolveotherwise healthy human males ofteninto pairs or rouleaux. My analyses alson response to selective pressure createdproduce a large proportion of sperm withrevealed that pairing most likely evolved onthree separate occasions, that conjugatesreverted ed to their ancestral aggregatedby the altered conditions in the femalereproductive tract. This prompted me toexamine the behavior of the conjugates“abnormal” morphology. My work strivesto understand why unusual variants insperm morphology occur and how thesecondition twice within the lineage withrouleaux, and that sperm dimorphismevolved a minimum of five times in divingbeetles, including both species whichdo and do not form conjugates. Fromin the females’ reproductive tracts.Conjugates were almost always foundwith their tips inserted into the exit duct(closest to the site of fertilization) and wereable to maintain this preferred position byvariations in form impact the fertility ofthe males that produce them.FALL 201115
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Fall 2011 - the Department of Biology - Syracuse University

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