International Journal of Ecology

Review Article

The Role of Parasitism in Adaptive Radiations—When Might Parasites Promote and When Might They Constrain Ecological Speciation?

Table 1

Empirical data speaking to evidence for a role of parasites in ecological speciation.
TaxonSystemSpecies statusEvidence for phylogenetic sister taxa?Divergence in parasite assemblage?Divergence in resistance traits?Does parasite-driven divergence precede other divergence?Is there parasite-mediated selection against immigrants?Is there parasite-mediated selection against hybrids?Is there assortative mating?Is there divergence in a potential revealing signal or MHC?Is divergent mate choice based on a revealing signal?Is divergent mate choice based on MHC-odours?The geography of divergenceRefs
FishThree-spine stickleback sympatric species pairs in Vancouver lakes (Canada)Reproductively isolated speciesYes in Paxton lake, no in Priest lakeYes, limnetic species have much more cestodes, fewer mollusks and different trematodesDivergence in MHC profilesNot knownNo dataNo dataYesYes, the limnetic species display redder male breeding dress and have lower MHC allele diversityYes, it is at least partly based on male breeding dressNot testedReinforcement after secondary contact[58, 91, 142]
Three-spine stickleback marine versus freshwater populations on Vancouver coast (Canada)Parapatric populations, perhaps speciesNo data, but very likelyNot known (but likely between the Sea and freshwaters)Freshwater residents are less susceptible than marines to infestation with freshwater parasites, the reverse is not knowNot knownYes, selection against marine immigrants operates in freshwaters; the reciprocal direction is not knownNo dataNot knownNot knownNot testedNot testedParapatric[70]
Three-spine stickleback marine versus freshwater species in ScotlandParapatric populations, perhaps speciesNo data, but very likelyYes, freshwater residents are heavily infested by a cestodeFreshwater residents are less susceptible than marines to infestation with freshwater parasites, the reverse is not knownNot knownYes, selection against marine immigrants operates in freshwaters; the reciprocal direction is not knownNo dataNot knownNot knownNot testedNot testedParapatric[70]
Three-spine stickleback
parapatric lake and river populations in Schleswig Holstein (Germany)		Parapatric populations, perhaps quite oldLake and stream populations are no direct sister taxa but belong to geographically more widespread reciprocally monophyletic cladesYes, lake populations harbor larger numbers of parasites compared to river populationsDivergence in MHC profiles, immunological parameters and habitat specific resistanceNot known, but unlikely given the wide geographical distribution of the lake and the stream cladeLikely, river ecotypes acquire higher parasite load in lake exposure compared to lake ecotype, but no difference in reciprocal river exposureNo, intermediates do not suffer increased susceptibility to parasitesYesYes, the lake population has larger MHC allele diversityNot testedYes: pleiotropy: pre-existing tendency for MHC complementarity causes female discrimination against too dissimilar males, that is, assortative mating.
indirect selection: female choice for locally resistant males		Parapatric[54–56, 92]
Three-spine stickleback, marine versus freshwater populations in Atlantic CanadaParapatric populationsNo dataYes, different parasite taxa are abundant in different environmentsDifferent MHC profiles between the populationsNot knownNo dataNo dataYesYes, different MHC allele frequencies between the populationsNot testedWeakly so, and labile to environmental conditionsParapatric[57]
Lake Victoria cichlids Pundamilia pundamilia and Pundamilia nyererei Complete speciation continuum, but parasites only studied at the complete speciation stageYes, from microsatellite and AFLP dataYes, different parasite taxa, but data available only for the complete speciation stage in speciation continuumNo dataNot known but perhaps not likely given that other traits diverge very early in the processNo dataNo dataYesYes, males of P. pundamilia show bright blue coloration and males of P. nyererei show bright red colorationFemale preference for male nuptial coloration, which appears to be a revealing signal at least in one of the speciesOlfaction is not required to maintain assortative matingGeographically sympatric, ecologically parapatric[10, 66, 101], Selz et al. Manuscript
Lake Malawi cichlids Pseudotropheus fainzilberi and P. emmiltos Reproductively isolated species with perhaps mild gene flowProbably not direct sister speciesYesDifferent MHC profiles between the populationsNot knownNo dataNo dataYesDivergent MHC profiles between the populationsNot knownIndirect evidence. Olfactory plays a role in mate choice which could mediate effects of divergent MHC profilesGeographically parapatric[67, 143, 144]
Alpine charr in NorwayConspecific parapatric populationsNo dataYes, profundal ecotype harbours significantly fewer infections compared to littoral/pelagic ecotypeNo dataNot knownNo dataNo dataYesNot knownNo testedNot testedParapatric[59]
Benthic and pelagic ecotypes of whitefish in two lakes in northern NorwayConspecific parapatric populationsNo dataYes, divergence in infections corresponds with the divergence in diet of the ecotypesNo dataNot knownNo dataNo dataYesNot knownNot testedNot testedParapatric[60]
Populations of guppies in TrinidadAllopatric/parapatric populations from different rivers with no reproductive isolationNo dataYes, populations were differently infected with Gyrodactylus monogeneansDifferent MHC allele frequencies among the populations, individuals carrying certain allele had fewer parasitesNot knownNo dataNo dataNot knownYes, different MHC allele frequencies between the populationsNot testedMHC could act as a homogenizing mechanism counteracting speciation among the populations although mechanisms is not testedAllopatric/ parapatric[40]
Whitefish in Swiss prealpine lakesComplete speciation (or speciation reversal) continuumYes, from microsatellite and AFLP dataYes, different parasite taxaNo dataNot known but divergence of parasite assemblage increases with genetic differentiationNo dataNo dataYes, inferred from microsatellite Fst in sympatryNo dataNot knownNot knownGeographically sympatric, ecologically parapatric[62, 145]
BirdMountain white-crowned sparrowsConspecific populationsNo data, but very likelyNo dataNo dataNot knownYes, immigrant individuals had higher infection rates and lower reproductive successNo, hybrids were at a selective advantageYes, partiallyNot known, but resident males sing a local dialectIt is based on song which might be a revealing signalNot testedParapatric[71, 75]
BirdCollared and pied flycatchersDistinct sympatric species with a hybrid zoneProbably, recently diverged speciesDifferences in infection rate between the speciesNo difference in immune responses between the speciesNot knownNo dataNo, hybrids had intermediate infection levels and immune responses compared to parent populationsYesNo dataNot testedNot testedSingle population[74]