Infectious disease in colonising population

A new study in Evol­u­tion Let­ters exper­i­ment­ally invest­ig­ated how pop­u­la­tion dynam­ics in col­on­ising pop­u­la­tions influ­ence the evol­u­tion of infec­tious dis­ease. Here, lead author Louise Nør­gaard describes the exper­i­ment­al approaches that led to the group’s inter­est­ing findings.

Infec­tious dis­ease is a major threat to human and wild­life well-being and epi­demi­olo­gic­al the­ory helps us under­stand how a patho­gen is expec­ted to spread through a pop­u­la­tion. Most host-patho­gen stud­ies, how­ever, have made the sim­pli­fy­ing assump­tion that the spread and evol­u­tion of dis­ease occurs in stable and non­dy­nam­ic host pop­u­la­tions. Wild host pop­u­la­tions are instead ever chan­ging and dynam­ic, with pop­u­la­tion growth rates and sizes fluc­tu­at­ing across time and space, as is seen when spe­cies expand their hab­it­at range, or in pop­u­la­tions with high extinc­tion and col­on­iz­a­tion rates. This lim­it­a­tion in our under­stand­ing of the mech­an­ism in play, when a patho­gen is con­fron­ted with col­on­iz­ing host pop­u­la­tions, was the major motiv­a­tion behind our study. This led us to per­form a range of labor­at­ory exper­i­ments to explore the influ­ence of host pop­u­la­tion dynam­ics on the per­form­ance of an invad­ing patho­gen at dif­fer­ent stages of the inva­sion pro­cess, from the ini­tial entry of an infec­ted car­ri­er into a pop­u­la­tion to the sub­sequent spread of new car­ri­ers to pop­u­la­tions elsewhere.

To do this, we needed a sys­tem in which we could con­trol a range of envir­on­ment­al, demo­graph­ic, and dis­ease related vari­ables. For this pur­pose, the water flea Daph­nia magna and its bac­teri­al gram-pos­it­ive patho­gen, Pas­teur­ia ramosa, appeared to be par­tic­u­larly use­ful. In this sys­tem, the clonally repro­du­cing host becomes infec­ted upon fil­ter-feed­ing, when spores are present in the water. The spores are then activ­ated inside the host, start to pro­lif­er­ate and fill up the host body cav­ity, and even­tu­ally kill the host. The spores are then released from the dying cada­ver, and a new infec­tion cycle can be ini­ti­ated. These dynam­ics allowed us to con­trol for genet­ic back­ground in the host, but also to tease apart the four para­site inva­sion steps, ran­ging from 1) ini­tial inva­sion of an infec­ted car­ri­er, 2) pro­lif­er­a­tion and pro­duc­tion of mature trans­mis­sion spores with­in the infec­ted host, 3) spread to new sus­cept­ible hosts (sec­ond­ary infec­tion) with­in the same pop­u­la­tion, and finally, 4) the para­site must spread between pop­u­la­tions to infect hosts in a patchy landscape.

With an exper­i­ment­al sys­tem in hand, we pro­ceeded to first explore how col­on­iz­a­tion dynam­ics in Daph­nia pop­u­la­tions arise as it spreads through a patchy land­scape. We seeded exper­i­ment­al patches that were con­nec­ted to a series of new and unin­hab­ited patches and mon­itored the growth in pop­u­la­tion size over time in each patch. We found char­ac­ter­ist­ic pop­u­la­tion dynam­ics con­sist­ing of an ini­tial phase of rap­id growth fol­lowed by a short phase of over­shoot, before finally reach­ing a stable car­ry­ing capa­city. Import­antly, those pop­u­la­tion dynam­ics were very dis­tinct and repeat­able between hab­it­at patches, allow­ing us to test dis­ease dynam­ics in each of the three host col­on­iz­a­tion phases.

In the next exper­i­ment, we tested the first two steps of the patho­gen infec­tion pro­cess; ini­tial estab­lish­ment and pro­lif­er­a­tion capa­city when con­fron­ted with each of the three char­ac­ter­ist­ic host col­on­iz­a­tion phases (rap­id growth, over­shoot, and sta­tion­ary phase). Here, we found that patho­gens gen­er­ally estab­lished with high­er suc­cess in host pop­u­la­tions that had just col­on­ized a new hab­it­at patch, but the five dif­fer­ent patho­gen gen­o­types tested differed in their suc­cess rates. Then we then quan­ti­fied the spore pro­duc­tion in patho­gens that suc­cess­fully estab­lished, and again found that most patho­gens had highest spore pro­duc­tion in recently estab­lished pop­u­la­tions, but with clear patho­gen spe­cif­ic responses.

This got us excited, and we moved on to explore the influ­ence of infec­tion on dis­pers­al beha­vi­or, and to under­stand wheth­er Daph­nia, like most humans, prefer to stay at home and rest when sick. We found that the beha­vi­or­al response to infec­tion was highly depend­ent on para­site gen­o­type; some para­sites reduced dis­pers­al rate of their host sig­ni­fic­antly, oth­ers barely influ­enced the rate at which indi­vidu­als moved through space. Most import­antly how­ever, the driv­ing factor in determ­in­ing how far an infec­ted car­ri­er moved appeared to be the lifespan; infec­tion reduced lifespan, and the patho­gen gen­o­types differed markedly in how quickly they killed their host and how much they impacted on dispersal.

Over­all, our res­ults show that patho­gen inva­sion fit­ness will be highest in newly col­on­ized host patches, but not all patho­gens will have the dis­pers­al capa­city to routinely exploit these tran­si­ent con­di­tions. Our res­ults sug­ges­ted that patho­gen traits optim­iz­ing patho­gen fit­ness in a grow­ing pop­u­la­tion may not be the same in a host pop­u­la­tion at car­ry­ing capa­city, and we iden­ti­fied a com­plex array of suc­cess­ful patho­gen strategies, depend­ing on the demo­graph­ic con­di­tions of the host pop­u­la­tion. This clearly demon­strated the poten­tial for dif­fer­ent patho­gen strategies or gen­o­types to be main­tained across a land­scape in which host pop­u­la­tion vary in their col­on­iz­a­tion his­tory or demography.

Louise Nør­gaard is a PhD can­did­ate in Dr Matt Hall’s lab at the School of Bio­lo­gic­al Sci­ences, Mon­ash Uni­ver­sity. The ori­gin­al study is freely avail­able to read and down­load at Evol­u­tion Letters.