Cost of Host Radiation in an RNA Virus

[Sally Furniss]

[SIZE=-1] Genetics, Vol. 156, 1465-1470, December 2000, Copyright ? 2000

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Cost of Host Radiation in an RNA Virus

Paul E. Turner^{<!-- null -->1,a} and Santiago F. Elena^a
[SIZE=-1] ^a Institut Cavanilles de Biodiversitat i Biolog?a Evolutiva and Departament de Gen?tica, Universitat de Val?ncia, 46071 Val?ncia, Spain [/SIZE] [SIZE=-1]Corresponding author: Santiago F. Elena, Institut Cavanilles de Biodiversitat i Biolog?a Evolutiva, Edifici d'Instituts de Paterna, Universitat de Val?ncia, Apartat 2085, 46071 Val?ncia, Spain., santiago.elena@uv.es<script type="text/javascript"><!-- var u = "santiago.elena", d = "uv.es"; document.getElementById("em0").innerHTML = '<a href="mailto:' + u + '@' + d + '">' + u + '@' + d + '<\/a>'//--></script> (E-mail)
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Abstract

Although host radiation allows a parasite to expand its ecological niche, traits governing the infection of multiple host types can decrease fitness in the original or alternate host environments. Reasons for this reduction in fitness include slower replication due to added genetic material or modifications, fitness trade-offs across host environments, and weaker selection resulting from simultaneous adaptation to multiple habitats. We examined the consequences of host radiation using vesicular stomatitis virus (VSV) and mammalian host cells in tissue culture. Replicate populations of VSV were allowed to evolve for 100 generations on the original host (BHK cells), on either of two novel hosts (HeLa and MDCK cells), or in environments where the availability of novel hosts fluctuated in a predictable or random way. As expected, each experimental population showed a substantial fitness gain in its own environment, but those evolved on new hosts (constant or fluctuating) suffered reduced competitiveness on the original host. However, whereas evolution on one novel host negatively correlated with performance on the unselected novel host, adaptation in fluctuating environments led to fitness improvements in both novel habitats.

[SIZE=+2] DISCUSSION[/SIZE] <table nowrap="" align="right" border="1" cellpadding="5"><tbody><tr><th align="left">[SIZE=-1]TOP
ABSTRACT
MATERIALS ND METHODS
RESULTS

DISCUSSION
LITERATURE CITED
[/SIZE]</th></tr></tbody></table> Does the radiation of parasites into novel host environmentsaffect their ability to compete on the original host? Do environmentsthat fluctuate in the availability of novel hosts limit adaptation?We examined the consequences of host radiation using VSV andmammalian host cells as a model system and these studies providethree pertinent results.
First, viruses that evolve on a novel host experience substantialimprovements in fitness, but show reduced competitive abilityin the original host. For viruses evolved on HeLa cells thefitness cost matched predictions; fitness of these populationson the original host was reduced below that of their ancestor.Evidently, traits that promote viral growth in cancerous epithelialcells (HeLa) oppose infection in fibroblast cells of connectivetissue (BHK). For viruses evolved on MDCK cells the cost wasless straightforward. These viruses retained strong competitiveability on the original host, but this negatively correlatedwith their performance on the evolved host. That is, the morefit evolved viruses were on MDCK, the worse they competed onBHK.
Second, adaptation of VSV to one novel host does not correlatewith improved performance on an unselected novel host. Whenviruses radiate into novel host environments, the possibilityexists that generally beneficial traits will fix in the population.For example, more rapid processing of RNA polymerase, increasedRNA polymerase affinity for the substrate, or an increased encapsidationefficiency will assist in replication in all hosts. In contrast,other traits, such as changes affecting membrane receptors,cellular cytoskeleton protein components, ribosomes, or Golgimembranes might only allow adaptation to a specific host. Ourresults suggest that cell-specific mutations tend to spreadin viral populations. HeLa-adapted viruses became less fit onMDCK, and MDCK-adapted strains became worse competitors on HeLa.Whereas these results support the general notion that fitnesstrade-offs across habitats drive species to specialize (<nobr>L[SIZE=-1]EVINS[/SIZE]1968 </nobr>), this result does not demonstrate a cost of host radiation,but rather it involves the specificity of viral adaptation toa particular host niche.
Third, simultaneous adaptation of viruses to two novel hostsdid not limit their ability to compete on each host separately.In contrast, viruses evolved in fluctuating habitats performedas well as those evolved in simple novel environments. Thiswas true whether environmental fluctuations in host availabilityoccurred in a random or correlated (predictable) fashion. Furthermore,previous experiments in eastern equine encephalitis virus (<nobr>W[SIZE=-1]EAVER[/SIZE]et al. 1999 </nobr>) and VSV (<nobr>N[SIZE=-1]OVELLA[/SIZE] et al. 1999 </nobr>) also show thatalternating host cycles do not limit adaptation. Taken together,these findings contradict the idea that weaker response to selection,or an increased mutational load, reduces the fitness of generalistsbelow that of specialists (<nobr>K[SIZE=-1]AWECKI[/SIZE] 1994 </nobr>, <nobr>K[SIZE=-1]AWECKI[/SIZE] 1998 </nobr>; <nobr>W[SIZE=-1]HITLOCK[/SIZE]1996 </nobr>).
We observed that fluctuating environments constrained the abilityof viruses to compete on their original host. Whereas MDCK-evolvedviruses maintained strong competitive ability on the ancestralhost, viruses evolved in fluctuating MDCK-HeLa environmentsdid not receive this benefit. Rather, fitness on the originalhost was reduced to that of viruses evolved on HeLa alone, demonstratingthat one of the two novel habitats determined competitive performance.For this reason, genetic changes involving adaptation to MDCKmust differ from those conferring an advantage in fluctuatingenvironments.
Selection for host expansion in VSV:
VSV infects mammals and insects and can be transmitted by arthropodvectors (<nobr>W[SIZE=-1]AGNER[/SIZE] 1991 </nobr>). Thus, exposure to novel and/or fluctuatinghost environments is likely to be important in VSV's evolution.This suggests that generalist variants of VSV capable of infectingmore than one host type are selectively favored at least fortransitions from old host to new hosts. Assuming that beneficialeffects of host radiation in VSV compensate for any associatedcosts, then an adaptive mechanism should facilitate VSV's abilityto jump between hosts. Perhaps host switches are simplifiedbecause VSV is an RNA virus that inherently mutates at veryhigh rates (<nobr>D[SIZE=-1]RAKE[/SIZE] and H[SIZE=-1]OLLAND[/SIZE] 1999 </nobr>); this may explain why thevast majority of arboviruses that alternate between hosts haveRNA genomes. In addition, one of the major limitations regardinghost range is the existence of appropriate receptors, and nicheexpansion may be easier for VSV because it seems to exploita receptor (phosphatidylserine) common to most animal cells(<nobr>W[SIZE=-1]AGNER[/SIZE] 1991 </nobr>).

http://www.genetics.org/cgi/content/full/156/4/1465