Bot­toms up: Ne­far­i­ous Ne­ma­todes and Red Rumps

by Michael Haar

Deep in the Ama­zon, a su­pervil­lain of mi­cro­scopic pro­por­tions strikes fear into the gan­glion of ho­nest tree-dwelling ants in every canopy. Myrme­conema neotrop­icum is a par­a­sitic ne­ma­tode, one of the count­less species in the phy­lum Ne­ma­toda that ex­ist in nearly every lo­ca­tion on Earth. For many, par­a­sitism is a topic that can elicit fas­ci­na­tion, laughs (Fig­ure 1), or hor­ror.

Fig­ure 1. Car­toon from Doc­tor Fun (04/25/06). Source

Com­pared to its other tetradone­matid brethren, Myr­me­co­ne­ma neotrop­icum stands out as a par­tic­u­larly de­vi­ous and re­source­ful round­worm. This ne­ma­tode in­fil­trates and es­tab­lishes an in­ti­mate hous­ing arrange­ment with its only known host, the South Amer­i­can ant Cephalotes at­ra­tus. Af­ter set­ting up shop in­side the ant and re­pro­du­cing, this tiny, thread-like squat­ter then pro­ceeds to make some dra­matic phys­i­o­log­i­cal changes while its host is none the wiser. The most shock­ing change oc­curs when the ne­ma­tode changes the ant's gaster – the cau­dal por­tion of the ab­domen (as seen in Fig­ure 2) – into a bul­bous berry that is ripe for the pick­ing (Fig­ure 3). Un­for­tunately for the ant, its new red rump only serves to pro­vide a col­or­ful tar­get for fruit-eat­ing birds pass­ing over­head.

This ne­ma­tode takes the role of be­ing a ma­nip­u­la­tive par­a­site to cre­ative new heights, al­ter­ing the phe­no­typic ex­pres­sion and be­hav­ior of the ant so it be­comes a fruit-mim­ic­k­ing ves­sel for the ne­ma­tode to board a bird and be re­leased through­out the rain for­est.

Par­a­sitism for Dum­mies: A Guide to Re­mod­el­ing Ant Gasters

Once the fer­til­ized eggs of Myrme­conema neotrop­icum are de­posited via bird fe­ces, they are picked up by worker ants for­ag­ing for food and brought to the colony. The ant lar­vae that are fed the bird poop also re­ceive a dose of the fer­til­ized ne­ma­tode eggs. In­side the in­fected lar­vae, the eggs hatch and the worms mi­grate to the ant gaster, where they ma­ture. Af­ter a larva ma­tures through the pu­pal stage, male and fe­male worms be­gin to cop­u­late. Males per­ish shortly af­ter mat­ing, but the fe­males live on to pro­duce hun­dreds of eggs in the gaster.

Fig­ure 2. The ba­sic anatomy of an ant. M. neotrop­icum is lo­cal­ized in the ant gaster. Source

An in­cred­i­ble se­ries of changes now takes place fol­low­ing the de­po­si­tion of Myrme­conema eggs in the ant's gaster. The typ­i­cal Cephalotes ant is a heav­ily ar­mored in­sect, called the "tur­tle ant" for good rea­son. In­fected ants look strik­ingly dif­fer­ent; their waxy black cu­ti­cle now turns a bright red (Fig­ure 3). A re­cent study pub­lished in The Jour­nal of Par­a­sitol­ogy spec­u­lates that a few pos­si­ble me­chanisms may be re­spon­si­ble for this trans­for­ma­tion: mor­pho­log­i­cal changes of the ex­oskele­ton or the tis­sues lin­ing the gaster; pro­duc­tion of new pig­ment or re­mov­ing ant melanin; or a com­bi­na­tion of these pos­si­bil­i­ties.

Arthro­pods like tur­tle ants are cov­ered by ex­oskele­tons. These suits of ar­mor are wo­ven to­gether from a lat­tice­work of var­i­ous pro­teins and lipids to form a cu­ti­cle bar­rier, us­ing a process called scle­ro­ti­za­tion. Ex­oskele­tons also serve as a source of nour­ish­ment for the ne­ma­tode. The re­sear­chers mea­sured the thick­ness of the ex­oskele­ton of in­fected and healthy ants us­ing scan­ning elec­tron mi­croscopy. This re­vealed quite a dif­fer­ence: the cu­ti­cle of in­fected ants was nearly 23% thin­ner than that of their healthy coun­ter­parts (Fig­ure 4).

Fig­ure 3a. An in­fected ant com­pared to a heal­thy ant (Fig. 3b). Its ab­domen is poised in the air, a red flare flag­ging down a free flight. Source

But would a thin­ner ex­oskele­ton in in­fected ants re­sult in such an un­usual color morph? As stated pre­vi­ously, a com­bi­na­tion of a thin­ner cu­ti­cle and the translo­ca­tion of pig­ment through the gaster eas­ily could. The sun­light pen­e­trat­ing the jun­gle canopy now passes through the thin­ner ant gaster, which like a prism now al­ters the light to pro­duce the red color. In tan­dem with the thin­ning of the cu­ti­cle, Myrme­conema may also be caus­ing a me­la­nin dis­rup­tion in an in­fected in­di­vid­ual. While we tend to think of melanin as im­por­tant for de­ter­min­ing hair or skin color, it is also an ex­tremely ver­sa­tile com­pound in a host of other or­gan­isms. In par­tic­u­lar, melanin plays a cru­cial role in the in­nate im­mune re­sponse of in­sects. When a mi­crobe in­vades an in­sect, its im­mune sys­tem is ac­ti­vated by com­po­nents unique to mi­crobes like lipopolysac­cha­rides or pep­ti­do­gly­cans (See Elio's in-depth de­scrip­tion on this im­mu­nity here). Sci­en­tists Cere­nius and Söder­häll also de­tail how me­lanin plays a cru­cial role in en­cap­su­lat­ing and de­stroy­ing pathogens in arthro­pods like the ant. It is pos­si­ble that the ne­ma­todes' ef­fect on the ant gaster not only thins the cu­ti­cle, but man­ages to shut off the pro­teinase sys­tem and other fac­tors like melanin that prove to be fa­tal to for­eign in­va­ders. Only fur­ther re­search could tell us by what means Myrme­conema dis­rupts the melaniza­tion process, but it has al­ready proven to have a for­mi­da­ble par­a­sitic toolkit at its dis­posal.

The par­a­site pup­pet-mas­ter

Fig­ure 3b. Cephalotes atra­tus ant. Photo by S. Yanoviak. Source

Par­a­sitism is a pow­er­ful force that in­flu­ences the be­hav­ior of the af­flicted host. Fol­low­ing in­fec­tion, Myr­me­co­ne­ma makes the in­dus­tri­ous tur­tle ant be­come noth­ing more than a clumsy ma­ri­o­nette. In­fected Cephalotes show en­tirely dif­fer­ent be­hav­iors com­pared to healthy ants: they be­come lethar­gic and fail to dis­play any of their char­ac­ter­is­tic alarm pheromones. Re­search con­duc­ted by S.P. Yanoviak and col­leagues showed that cer­tain mor­pho­log­i­cal changes are as­so­ci­ated with the strange be­hav­ior of the in­fected ants. By dis­sect­ing the gasters of in­fected in­di­vid­u­als, they found that the ven­tral nerve cord was con­sis­tently at­ro­phied, and that a unique struc­ture called the post­peti­ole junc­tion that links the ab­domen to the ant's tho­rax was also com­promised. This caused the red "berry-gaster" to read­ily de­tach from the ant, likely due to the weight of the pay­load the ant has to carry. The re­searchers hy­poth­e­sized that an­other for­ager ant could eas­ily pick up the gaster (with­out dis­man­tling its com­rade) and bring it home – an­other means to con­tinue the ne­ma­tode life­cy­cle. The ad­di­tional weight of the gaster and com­pro­mised mo­tor func­tion of the in­fected ant make pre­da­tion rates in­crease sig­nif­i­cantly. In­ter­est­ingly enough, de­spite the added weight of the ne­ma­tode eggs (the in­fected are up to 40% heav­ier), the par­a­site im­poses no dis­cernible meta­bolic cost for its host com­pared to healthy Cephalotes atra­tus ants.

The re­la­tion­ship of Myrme­conema neotrop­icum with Cephalotes atra­tus is highly spe­cific. Some sci­en­tists are ea­ger to point out that this par­a­sitic as­so­ci­a­tion is the per­fect ex­am­ple of an "ex­ten­ded phe­no­type", a term coined by famed writer Richard Dawkins. In this case, the tiny ne­ma­tode has evolved to ma­nip­u­late the be­hav­ior of its host (the ant) via fruit mim­icry just for the sake of im­prov­ing its own fit­ness. The no­tion of an ex­tended phe­no­type be­comes even more com­pli­cated when an in­ter­me­di­ate host, like the bird, is in­tro­duced into the equa­tion. Though the bird does not di­rectly trans­mit the par­a­site to the tur­tle ant, it is worth men­tion­ing that it serves to in­crease the dis­per­sal of the par­a­site amongst the ant pop­u­la­tion.

Fig­ure 4. Av­er­age ex­oskele­tal thick­ness of the head and gaster of healthy and in­fected tur­tle ants. Head (n = 34); Gaster (n = 36). Source

The mod­i­fi­ca­tion of a host's be­hav­ior by a par­a­site is the sub­ject of con­sid­er­able in­ter­est and the­o­ret­i­cal scrutiny. While a hand­ful of par­a­sites are stud­ied in­tently in ve­te­ri­na­ry med­i­cine and agri­cul­tural sci­ence, oth­ers like Myr­me­co­ne­ma con­tinue to op­er­ate in the shad­ows, ex­ploi­ting the in­ter­nal ma­chin­ery of the ant in ways that are still un­clear to re­searchers. Re­gard­less of the­ory, I can­not help but mar­vel at the mul­ti­ple phys­i­o­log­i­cal and be­hav­ioral ef­fects that Myrme­conema neotrop­icum im­poses on the Cephalotes atra­tus ant. It truly is the ul­ti­mate pa­ra­si­tic vil­lain (or hero, if you pre­fer)!

 

Mike is a na­tive of Buf­falo, NY. A new grad­u­ate of Can­i­sius Col­lege, he stud­ied An­i­mal Be­hav­ior and Ecol­ogy, and dur­ing his se­nior year he had the op­por­tu­nity to take the mi­cro­bi­ol­ogy class taught by STC As­so­ciate Blog­ger Daniel Haeusser. The class helped kin­dle a pas­sion for the weird and won­der­ful world of mi­crobes and a new ap­pre­ci­a­tion for the pro­kar­yo­tes that of­ten get ig­nored in gen­eral bi­ol­ogy. Work­ing at a small an­i­mal hos­pi­tal and hav­ing pre­vi­ous ex­pe­ri­ence at a zoo, Mike gets to see a va­ri­ety of mi­cro­bial and par­a­sitic af­flic­tions up close and it is for this rea­son that he loves to read and write about para­si­to­lo­gy. In the fu­ture, Mike plans to at­tend vet­eri­nary school while con­tin­u­ing to learn about the bur­geon­ing field of mi­cro­bi­ol­ogy.