Novel trophic niches drive variable progress towards ecological speciation within an adaptive radiation of pupfishes

Adaptive radiation is recognized by a rapid burst of phenotypic, ecological and species diversification. However, it is unknown whether different species within an adaptive radiation evolve reproductive isolation at different rates. We compared patterns of genetic differentiation between nascent species within an adaptive radiation of Cyprinodon pupfishes using genotyping by sequencing. Similar to classic adaptive radiations, this clade exhibits rapid morphological diversification rates and two species are novel trophic specialists, a scale‐eater and hard‐shelled prey specialist (durophage), yet the radiation is <10 000 years old. Both specialists and an abundant generalist species all coexist in the benthic zone of lakes on San Salvador Island, Bahamas. Based on 13 912 single‐nucleotide polymorphisms (SNPs), we found consistent differences in genetic differentiation between each specialist species and the generalist across seven lakes. The scale‐eater showed the greatest genetic differentiation and clustered by species across lakes, whereas durophage populations often clustered with sympatric generalist populations, consistent with parallel speciation across lakes. However, we found strong evidence of admixture between durophage populations in different lakes, supporting a single origin of this species and genome‐wide introgression with sympatric generalist populations. We conclude that the scale‐eater is further along the speciation‐with‐gene‐flow continuum than the durophage and suggest that different adaptive landscapes underlying these two niche environments drive variable progress towards speciation within the same habitat. Our previous measurements of fitness surfaces in these lakes support this conclusion: the scale‐eating fitness peak may be more distant than the durophage peak on the complex adaptive landscape driving adaptive radiation.     

The species flocks of lacustrine gastropods: <Emphasis Type="Italic">Tylomelania</Emphasis> on Sulawesi as models in speciation and adaptive radiation

Endemic radiations provide splendid opportunities for studies in evolutionary biology. Species flocks in ancient lakes, such as in Tanganyika, Malawi or Baikal, have featured prominently in evolutionary biology, viewing these “evolutionary theatres” as hotspots of diversification. However, following a century of neglect, the endemic evolution of limnic cerithioidean gastropods in the two central lake systems on the Indonesian island of Sulawesi (i.e. Lake Poso and the lakes of the Malili system, e.g. Danau Matano, Mahalona and Towuti) also provide instructive model cases for the study of speciation mechanisms, adaptive radiation and annidation (i.e. niche exploitation). We here discuss the evolutionary and taxonomic implications of the lacustrine species flocks in Tylomelania from these lakes in Sulawesi as an exceptional endemic assemblage of morphologically distinct viviparous pachychilid gastropods. This first comprehensive compilation of data on both ancient lake systems, Poso and Malili, offers a new perspective on ecological differentiation in this radiation. Presented here within the framework of the theory of evolutionary ecology it provides a research program for acquiring a synthetical perspective that includes morphology, molecular genetics, ecology and biogeography. In this context, it will be possible to compare the species flocks of these truly “Darwinian snails” on Sulawesi with the long enigmatic, so-called thalassoid (i.e. marine-like) gastropod radiation in East African’s Lake Tanganyika.     

Genetic structure and connectivity among lake populations of threatened Paratherina sailfin silversides from Sulawesi, Indonesia

Spatially restricted endemic species are of special conservation concern as their narrow distributions render them particularly vulnerable to extinction through habitat loss. However, estimates of connectivity among populations can provide a basis for targeted conservation action. Here we quantify population genetic structure and connectivity for two endemic Sailfin silverside species within and among two lakes from the Malili Lakes, Indonesia. For both species, a greater proportion of genetic variance was found among sites within a lake than between lakes, indicative of riverine gene flow and cryptic genetic structure within the lakes. Bayesian genotype clustering revealed substantial population genetic structure within and among lakes, but also showed evidence of dispersal between lakes. These results are timely given the growing anthropogenic stressors in the Malili Lakes watershed, including mining and forestry operations.     

The ancient lakes of Indonesia: towards integrated research on speciation

Ancient lakes have provided considerable insights into the drivers of speciation and adaptive radiation in aquatic organisms. Most studies of species-flocks, however, focus only on a single group of organisms, and few have attempted to integrate geological, limnological, ecological, and genetic drivers of speciation on multiple species-flocks at various trophic levels. As such, there is a need for a comprehensive model system for research on speciation in aquatic environments where multiple radiations are investigated at various levels of biological organization (e.g., individual, population, and ecosystem) and placed in light of geographical and geological setting. The ancient Malili Lakes of Sulawesi, Indonesia, are ideal candidates for such a model, and represent the only hydrologically connected ancient lakes in the world. These lakes are characterized by ultra-oligotrophy and unique physicochemical conditions that govern the composition and production of planktonic communities. At higher trophic levels, there are three recurring trends: (1) low taxonomic richness and simple community structures, (2) adaptive radiations with trophic specialization, and (3) remarkably high endemism with evolutionary innovations throughout the lakes and species-flocks. Furthermore, the restricted geographic distributions of species-flocks within the Malili Lakes indicate that each lake constitutes a unique environment, and dispersal among lakes is limited, despite close contemporary connectivity. These observations suggest that ecological and evolutionary processes are regulated from the bottom up, and speciation is primarily facilitated by interspecific and intraspecific competition for limited resources. The Malili Lakes represent an outstanding natural model for integrative research into speciation as they offer the opportunity to explore the roles of geography, dispersal, and selection in the radiation of aquatic organisms.     

Escalation and trophic specialization drive adaptive radiation of freshwater gastropods in ancient lakes on Sulawesi, Indonesia

Species flocks in ancient lakes have long been appreciated as ideal model systems for the study of speciation and adaptive processes. We here present data from a new invertebrate model system with intrinsic parameters distinct from those of other documented radiations. The ancient lakes on Sulawesi harbour an endemic species flock of at least 33 species of viviparous snails. Molecular data reveal multiple independent colonizations of the lakes by riverine ancestors. In each colonizing clade, parallel evolution of conspicuous shell morphologies, followed by a differentiation of trophic morphology and the development of habitat specificity can be observed. Extensive shell crushing experiments and strong dentition of the chelae observed in some lacustrine crab species suggest that coevolution with crabs, i.e. escalation, is the most likely cause of initial shell divergence. By contrast, repeated parallel evolution in radula morphology indicates that speciation within lineages is driven by divergent adaptation to different resources among sympatric taxa. The inclusion of coevolutionary processes is unique in this system compared with diversification models developed for vertebrate radiations.     

Distinct colonization waves underlie the diversification of the freshwater sculpin (Cottus gobio) in the Central European Alpine region

Ecological speciation and adaptive radiation are key processes shaping northern temperate freshwater fish diversity. Both often involve parapatric differentiation between stream and lake populations and less often, sympatric intralacustrine diversification into habitat‐ and resource‐associated ecotypes. However, few taxa have been studied, calling for studies of others to investigate the generality of these processes. Here, we test for diversification within catchments in freshwater sculpins in a network of peri‐Alpine lakes and streams. Using 8047 and 13 182 restriction site‐associated (RADseq) SNPs, respectively, we identify three deeply divergent phylogeographic lineages associated with different major European drainages. Within the Aare catchment, we observe populations from geographically distant lakes to be genetically more similar to each other than to populations from nearby streams. This pattern is consistent with two distinct colonization waves, rather than by parapatric ecological speciation after a single colonization wave. We further find two distinct depth distribution modes in three lakes of the Aare catchment, one in very shallow and one in very deep water, and significant genomewide differentiation between these in one lake. Sculpins in the Aare catchment appear to represent an early‐stage adaptive radiation involving the evolution of a lacustrine lineage distinct from parapatric stream sculpins and the repeated onset of depth‐related intralacustrine differentiation.     

Niche divergence facilitated by fine‐scale ecological partitioning in a recent cichlid fish adaptive radiation

Ecomorphological differentiation is a key feature of adaptive radiations, with a general trend for specialization and niche expansion following divergence. Ecological opportunity afforded by invasion of a new habitat is thought to act as an ecological release, facilitating divergence, and speciation. Here, we investigate trophic adaptive morphology and ecology of an endemic clade of oreochromine cichlid fishes (Alcolapia) that radiated along a herbivorous trophic axis following colonization of an isolated lacustrine environment, and demonstrate phenotype‐environment correlation. Ecological and morphological divergence of the Alcolapia species flock are examined in a phylogenomic context, to infer ecological niche occupation within the radiation. Species divergence is observed in both ecology and morphology, supporting the importance of ecological speciation within the radiation. Comparison with an outgroup taxon reveals large‐scale ecomorphological divergence but shallow genomic differentiation within the Alcolapia adaptive radiation. Ancestral morphological reconstruction suggests lake colonization by a generalist oreochromine phenotype that diverged in Lake Natron to varied herbivorous morphologies akin to specialist herbivores in Lakes Tanganyika and Malawi.     

AN ADAPTIVE RADIATION OF FROGS IN A SOUTHEAST ASIAN ISLAND ARCHIPELAGO

Living amphibians exhibit a diversity of ecologies, life histories, and species‐rich lineages that offers opportunities for studies of adaptive radiation. We characterize a diverse clade of frogs (Kaloula, Microhylidae) in the Philippine island archipelago as an example of an adaptive radiation into three primary habitat specialists or ecotypes. We use a novel phylogenetic estimate for this clade to evaluate the tempo of lineage accumulation and morphological diversification. Because species‐level phylogenetic estimates for Philippine Kaloula are lacking, we employ dense population sampling to determine the appropriate evolutionary lineages for diversification analyses. We explicitly take phylogenetic uncertainty into account when calculating diversification and disparification statistics and fitting models of diversification. Following dispersal to the Philippines from Southeast Asia, Kaloula radiated rapidly into several well‐supported clades. Morphological variation within Kaloula is partly explained by ecotype and accumulated at high levels during this radiation, including within ecotypes. We pinpoint an axis of morphospace related directly to climbing and digging behaviors and find patterns of phenotypic evolution suggestive of ecological opportunity with partitioning into distinct habitat specialists. We conclude by discussing the components of phenotypic diversity that are likely important in amphibian adaptive radiations.     

Ancient lakes as hotspots of diversity: a morphological review of an endemic species flock of <Emphasis Type="Italic">Tylomelania</Emphasis> (Gastropoda: Cerithioidea: Pachychilidae) in the Malili lake system on Sulawesi,Indonesia

The viviparous freshwater gastropod Tylomelania (Caenogastropoda: Cerithioidea: Pachychilidae) endemic to the Indonesian island Sulawesi has radiated extensively in two ancient lake systems. We here present the first systematic species-level review of taxa in the five lakes of the Malili lake system, which contains the most diverse and best studied freshwater fauna on Sulawesi. Our results indicate a significantly higher diversity of Tylomelania in these lakes than previously perceived based on morphological evidence for delimiting the taxa. We describe nine new species, thus increasing the number of taxa known from the Malili lakes to 25. Tylomelania species are inhabiting all available substrates in the lakes, and the diversity of habitats is reflected in an unparalleled range of radula types in this closely related group. Several species show a high intraspecific variability in some characters, and their closer investigation will probably lead to the discovery of more cryptic species. As it is, this species flock on Sulawesi is among the largest freshwater mollusc radiations known. Since the Malili lake system also contains other large endemic species flocks of e.g. crustaceans and fishes, it is a major hotspot of freshwater biodiversity in Asia to become a conservation priority. Handling editor: K. Martens     

Phylogenetic conservation of freshwater lake habitat preference varies between abundant bacterioplankton phyla

Despite their homogeneous appearance, aquatic systems harbour heterogeneous habitats resulting from nutrient gradients, suspended particulate matter and stratification. Recent reports suggest phylogenetically conserved habitat preferences among bacterioplankton, particularly for particle‐associated (PA) and free‐living (FL) habitats. Here, we show that independent of lake nutrient level and layer, PA and FL abundance‐weighted bacterial community composition (BCC) differed and that inter‐lake BCC varied more for PA than for FL fractions. In low‐nutrient lakes, BCC differences between PA and FL fractions were larger than those between lake layers. The reverse was true for high‐nutrient lakes. Nutrient level affected BCC more in hypolimnia than in epilimnia, likely due to hypolimnetic hypoxia in high‐nutrient lakes. In line with previous reports, we observed within‐phylum operational taxonomic unit (OTU) habitat preference conservation, although not for all phyla, including the phylum with the highest average relative abundance across all habitats (Bacteroidetes). Consistent phylum‐level habitat preferences may indicate that the functional traits that underpin ecological adaptation of freshwater bacteria to lake habitats can be phylogenetically conserved, although the levels of conservation are phylum dependent. Resolving taxa preferences for freshwater habitats sets the stage for identification of traits that underpin habitat specialization and associated functional traits that influence differences in biogeochemical cycling across freshwater lake habitats.     

Variable extent of parallelism in respiratory,circulatory, and neurological traits across lake whitefish species pairs

Parallel adaptive radiation events provide a powerful framework for investigations of ecology's contribution to phenotypic diversification. Ecologically driven divergence has been invoked to explain the repeated evolution of sympatric dwarf and normal lake whitefish (Coregonus clupeaformis) species in multiple lakes in eastern North America. Nevertheless, links between most putatively adaptive traits and ecological variation remain poorly defined within and among whitefish species pairs. Here, we examine four species pairs for variation in gill, heart, and brain size; three traits predicted to show strong phenotypic responses to ecological divergence. In each of the species pairs, normals exhibited larger body size standardized gills compared to dwarfs – a pattern that is suggestive of a common ecological driver of gill size divergence. Within lakes, the seasonal hypoxia experienced in the benthic environment is a likely factor leading to the requirement for larger gills in normals. Interestingly, the morphological pathways used to achieve larger gills varied between species pairs from Québec and Maine, which may imply subtle non‐parallelism in gill size divergence related to differences in genetic background. There was also a non‐significant trend toward larger hearts in dwarfs, the more active species of the two, whereas brain size varied exclusively among the lake populations. Taken together, our results suggest that the diversification of whitefish has been driven by parallel and non‐parallel ecological conditions across lakes. Furthermore, the phenotypic response to ecological variation may depend on genetic background of each population.     

Crater lake cichlids individually specialize along the benthic–limnetic axis

A common pattern of adaptive diversification in freshwater fishes is the repeated evolution of elongated open water (limnetic) species and high‐bodied shore (benthic) species from generalist ancestors. Studies on phenotype‐diet correlations have suggested that population‐wide individual specialization occurs at an early evolutionary and ecological stage of divergence and niche partitioning. This variable restricted niche use across individuals can provide the raw material for earliest stages of sympatric divergence. We investigated variation in morphology and diet as well as their correlations along the benthic‐limnetic axis in an extremely young Midas cichlid species, Amphilophus tolteca, endemic to the Nicaraguan crater lake Asososca Managua. We found that A. tolteca varied continuously in ecologically relevant traits such as body shape and lower pharyngeal jaw morphology. The correlation of these phenotypes with niche suggested that individuals are specialized along the benthic‐limnetic axis. No genetic differentiation within the crater lake was detected based on genotypes from 13 microsatellite loci. Overall, we found that individual specialization in this young crater lake species encompasses the limnetic‐ as well as the benthic macro‐habitat. Yet there is no evidence for any diversification within the species, making this a candidate system for studying what might be the early stages preceding sympatric divergence.     

Allopatric and sympatric diversification within roach (Rutilus rutilus) of large pre‐alpine lakes

Intraspecific differentiation in response to divergent natural selection between environments is a common phenomenon in some northern freshwater fishes, especially salmonids and stickleback. Understanding why these taxa diversify and undergo adaptive radiations while most other fish species in the same environments do not, remains an open question. The possibility for intraspecific diversification has rarely been evaluated for most northern freshwater fish species. Here, we assess the potential for intraspecific differentiation between and within lake populations of roach (Rutilus rutilus)—a widespread and abundant cyprinid species—in lakes in which salmonids have evolved endemic adaptive radiations. Based on more than 3,000 polymorphic RADseq markers, we detected low but significant genetic differentiation between roach populations of two ultraoligotrophic lakes and between these and populations from other lakes. This, together with differentiation in head morphology and stable isotope signatures, suggests evolutionary and ecological differentiation among some of our studied populations. Next, we tested for intralacustrine diversification of roach within Lake Brienz, the most pristine lake surveyed in this study. We found significant phenotypic evidence for ecological intralacustrine differentiation between roach caught over a muddy substrate and those caught over a rocky substrate. However, evidence for intralacustrine genetic differentiation is at best subtle and phenotypic changes may therefore be mostly plastic. Overall, our findings suggest roach can differ between ecologically distinct lakes, but the extent of intralacustrine ecological differentiation is weak, which contrasts with the strong differentiation among endemic species of whitefish in the same lakes.     

Disruptive natural selection predicts divergence between the sexes during adaptive radiation

Evolution of sexual dimorphism in ecologically relevant traits, for example, via resource competition between the sexes, is traditionally envisioned to stall the progress of adaptive radiation. An alternative view is that evolution of ecological sexual dimorphism could in fact play an important positive role by facilitating sex‐specific adaptation. How competition‐driven disruptive selection, ecological sexual dimorphism, and speciation interact during real adaptive radiations is thus a critical and open empirical question. Here, we examine the relationships between these three processes in a clade of salamanders that has recently radiated into divergent niches associated with an aquatic life cycle. We find that morphological divergence between the sexes has occurred in a combination of head shape traits that are under disruptive natural selection within breeding ponds, while divergence among species means has occurred independently of this disruptive selection. Further, we find that adaptation to aquatic life is associated with increased sexual dimorphism across taxa, consistent with the hypothesis of clade‐wide character displacement between the sexes. Our results suggest the evolution of ecological sexual dimorphism may play a key role in niche divergence among nascent species and demonstrate that ecological sexual dimorphism and ecological speciation can and do evolve concurrently in the early stages of adaptive radiation.     

Radiating in a river: systematics, molecular genetics and morphological differentiation of viviparous freshwater gastropods endemic to the Kaek River, central Thailand (Cerithioidea, Pachychilidae)

Speciation in the context of adaptive radiation is regarded as a key process in the creation of biodiversity. While several lacustrine species flocks provide ideal models for elucidating the underlying evolutionary mechanisms, riverine radiations are both rarely known and studied. The Kaek River, a third‐order tributary of the Nan River and Chao Praya drainage in central Thailand, harbours an exceptional endemic species assemblage of morphologically distinct, viviparous pachychilid gastropods. Our systematic revision, combining a morphological and molecular genetics approach, reveals the sympatric existence of at least seven species of the genus Brotia that is widespread in rivers of South‐east Asia where usually only two species at the most coexist. At eight locations along a 100‐kilometre stretch of the Kaek River, we found the syntopic occurrence of two to three species that are separated by specific habitat preferences and exhibit trophic specialization in their radula morphology. Phylogenetic analyses (using MP, NJ, ML and Bayesian inference statistics) of partial COI and 16S sequence data of 17 samples from six species occurring sympatrically and parapatrically, respectively, in the Kaek River drainage (plus the type species B. pagodula as outgroup) indicate monophyly of all these endemic species. Brotia solemiana, which also occurs in the Loei River, a tributary of the Mekong drainage system, was found to be sister to all other Kaek River pachychilids. The distinctive morphotypes, proposed here to represent biospecies, do not show high levels of genetic variation consistent with long periods of reproductive isolation. This suggests a relatively recent origin of this intrariverine radiation and rapid morphological divergence in the Kaek River Brotia. Recent diversification combined with ecological separation and trophic specialization parallels conditions found, albeit on a more specious level, in the lacustrine species flock of the closely related pachychilid genus Tylomelania, which is endemic to ancient lakes on the Indonesian island of Sulawesi. We discuss and compare the allopatric and ecological aspects of speciation in this unique riverine radiation and outline a putative historical biogeography of the Kaek River species, employing the most recent geological and palaeohydrological data for Thailand. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82 , 275–311.     

Role of ancient lakes in genetic and phenotypic diversification of freshwater snails

Endemic organisms of ancient lakes have been studied as models to understand processes of speciation and adaptive radiation. However, it remains unclear how ancient lakes play roles in genetic and phenotypic diversity of freshwater mollusks. In the present study, we focus on viviparid freshwater snails in the ancient lakes of East and Southeast Asia (Japan and China) to address this question. Using molecular phylogenetic analyses based on mitochondrial (COI, 16S) and nuclear genes (18S, 28S, H3), we show that patterns of species diversification in viviparid lineages. Colonization to ancient lakes occurred independently in China and Japan at least four times, with subsequent diversification into more than two species within each lake group. Morphological analyses of fossil related viviparids suggest parallel phenotypic evolution occurred in the different lakes and ages. Each lake contained a single lineage which was phenotypically diversified relative to those from other sites. Using genome‐wide SNPs obtained by MIG‐seq, we also examined the genetic structure of three Japanese viviparids, including two endemic species of ancient Lake Biwa. The results suggest that these two species diversified from the population of the third species living in wetlands surrounding the lake. These findings suggest that rapid diversification of lineages and phenotypic divergence can occur in ancient lakes compared to other habitats. Formation of large lakes probably promotes speciation and phenotypic divergence as a result of adaptation into different microhabitats. High numbers of ancient lakes could be a driver of species diversity in Asian viviparid snails.     

Bony labyrinth morphometry reveals hidden diversity in lungless salamanders (Family Plethodontidae): Structural correlates of ecology,development, and vision in the inner ear

Lungless salamanders (Family Plethodontidae) form a highly speciose group that has undergone spectacular adaptive radiation to colonize a multitude of habitats. Substantial morphological variation in the otic region coupled with great ecological diversity within this clade make plethodontids an excellent model for exploring the ecomorphology of the amphibian ear. We examined the influence of habitat, development, and vision on inner ear morphology in 52 plethodontid species. We collected traditional and 3D geometric morphometric measurements to characterize variation in size and shape of the otic endocast and peripheral structures of the salamander ear. Phylogenetic comparative analyses demonstrate structural convergence in the inner ear across ecologically similar species. Species that dwell in spatially complex microhabitats exhibit robust, highly curved semicircular canals suggesting enhanced vestibular sense, whereas species with reduced visual systems demonstrate reduced canal curvature indicative of relaxed selection on the vestibulo‐ocular reflex. Cave specialists show parallel enlargement of auditory‐associated structures. The morphological correlates of ecology among diverse species reveal underlying evidence of habitat specialization in the inner ear and suggest that there exists physiological variation in the function of the salamander ear even in the apparent absence of selective pressures on the auditory system to support acoustic behavior.     

CORRELATED TROPHIC SPECIALIZATION AND GENETIC DIVERGENCE IN SYMPATRIC LAKE WHITEFISH ECOTYPES (COREGONUS CLUPEAFORMIS): SUPPORT FOR THE ECOLOGICAL SPECIATION HYPOTHESIS

There is ample empirical evidence that phenotypic diversification in an adaptive radiation is the outcome of divergent natural selection related to differential resource use. In contrast, the role of ecological forces in favoring and maintaining reproductive isolation in nature remains poorly understood. If the same forces driving phenotypic divergence are also responsible for speciation, one would predict a correlation between the extent of trophic specialization (reflecting variable intensity of divergent natural selection) and that of reproductive isolation being reached in a given environment. We tested this hypothesis by comparing the extent of morphological and genetic differentiation between sympatric dwarf and normal whitefish ecotypes (Coregonus sp.) from six lakes of the St. John River basin (eastern Canada and northern Maine). Eight meristic variables, 19 morphometric variables, and six microsatellite loci were used to quantify morphological and genetic differentiation, respectively. Dwarf and normal ecotypes in each lake differed primarily by traits related to trophic specialization, but the extent of differentiation varied among lakes. Significant but variable genetic divergence between ecotypes within lakes was also observed. A negative correlation was observed between the extent of gene flow between ecotypes within a lake and that of their morphological differentiation in trophic-related traits. The extent of reproductive isolation reached between dwarf and normal whitefish ecotypes appears to be driven by the potential for occupying distinct trophic niches and, thus, by the same selective forces driving tropic specialization in each lake. These results therefore support the hypothesis of ecological speciation.     

Divergent parasite infections in sympatric cichlid species in Lake Victoria

Parasitism has been proposed as a factor in host speciation, as an agent affecting coexistence of host species in species‐rich communities and as a driver of post‐speciation diversification. Young adaptive radiations of closely related host species of varying ecological and genomic differentiation provide interesting opportunities to explore interactions between patterns of parasitism, divergence and coexistence of sympatric host species. Here, we explored patterns in ectoparasitism in a community of 16 fully sympatric cichlid species at Makobe Island in Lake Victoria, a model system of vertebrate adaptive radiation. We asked whether host niche, host abundance or host genetic differentiation explains variation in infection patterns. We found significant differences in infections, the magnitude of which was weakly correlated with the extent of genomic divergence between the host species, but more strongly with the main ecological gradient, water depth. These effects were most evident with infections of Cichlidogyrus monogeneans, whereas the only host species with a strictly crevice‐dwelling niche, Pundamilia pundamilia, deviated from the general negative relationship between depth and parasitism. In accordance with the Janzen–Connell hypothesis, we also found that host abundance tended to be positively associated with infections in some parasite taxa. Data on the Pundamilia sister species pairs from three other islands with variable degrees of habitat (crevice) specialization suggested that the lower parasite abundance of P. pundamilia at Makobe could result from both habitat specialization and the evolution of specific resistance. Our results support influences of host genetic differentiation and host ecology in determining infections in this diverse community of sympatric cichlid species.