Cost of morphological specialization: feeding performance of the two morphs in the trophically polymorphic cichlid fish,Cichlasoma citrinellum

Summary The feeding performance on soft and hard prey of two morphs of the trophically polymorphic Neotropical cichlid fish, Cichlasoma citrinellum, was investigated in the laboratory. The molariform morphs, specialized to feed on hard prey, are able to crack snail shells that are twice as hard as those cracked by the papilliform morphs. During ecological bottlenecks in food resources this ability should allow molariform morphs to exploit alternate, less preferred prey sources that are not available to papilliform morphs. Analysis of stomach contents revealed that molariform morphs feed significantly more often on hard snails than do papilliform morphs (Meyer 1989a). The performance advantage of the trophically specialized morphs when feeding on hard prey is countered by their less efficient performance on soft diets. The morphologically generalized papilliform morph feeds more efficiently on soft prey. The abundance of preferred soft prey, seasonal fluctuations in prey availability and the frequency of ecological bottlenecks may determine the relative abundance of these two morphs in natural populations in Nicaraguan lakes.     

Geometric Morphometric Analysis of Body-Form Variability in Cichlasoma minckleyi, the Cuatro Cienegas cichlid

In this study, I investigate body-form variability in the trophically polymorphic Cuatro Cienegas cichlid, Cichlasoma minckleyi. I use geometric morphometrics to assess and compare size, shape, and allometric patterns within and between dental morphs (distinguished by differences in pharyngeal bones and papilliform or molariform dentitions). I find that dental morphs do not differ significantly in size, shape, or allometric slopes, but do differ in allometric intercepts; thus, dental morphs exhibit different patterns of body-form variability. Within each morph, body-form varies between more fusiform 'piscivores' and deeper-bodied dietary generalists. However, papilliform individuals show a continuous distribution of body-forms, whereas molariform individuals exhibit a discontinuity. I compare results from geometric analyses with those from a traditional (distance-based) morphometric analysis, finding that geometric techniques more clearly recognize discontinuities in shape. Finally, I suggest explanations for observed differences in body-form variability between dental morphs, concluding that the best explanation hinges on the relative importance of genetic and environmental factors in influencing body-form.     

Feeding specialization in Herichthys minckleyi: a trophically polymorphic fish

Diet specialization in the trophically polymorphic cichlid fish Herichthys minckleyi was examined using gut contents. Individual H. minckleyi were categorized as having molariform, papilliform or undetermined pharyngeal jaws. The presence of enlarged flattened pharyngeal jaw teeth was used to categorize H. minckleyi as molariform, and the possession of only small pencil‐like pharyngeal teeth was used to classify fish as papilliform. Undetermined individuals (<50 mm standard length, L _S) were not assigned to one of the two larger morphotypes. Arthropods were found to be generally rare in H. minckleyi gut contents, but when present, they were most frequently recovered from undetermined individuals. The percentage of plant material consumed by undetermined H. minckleyi was not as great as papilliforms ingested on average, and snail crushing by undetermined H. minckleyi was not evident. A significantly greater mean percentage of plant detritus was recovered from papilliforms compared to molariforms. Snails were crushed by molariforms more frequently than by papilliforms. When only molariforms and papilliforms that had crushed snails were compared, a greater number of snails were crushed by molariforms. No relationship was found between molariform L _S and the number of snails crushed, but greater molariform tooth number, adjusted for L _S, was indicative of recent snail crushing. The maintenance of H. minckleyi pharyngeal jaw variation could be promoted by intraspecific diet differentiation.     

Micro- and macroevolutionary decoupling of cichlid jaws: a test of Liem's key innovation hypothesis

The extent to which elements of functional systems can change independently (modularity) likely influences the diversification of lineages. Major innovations in organismal design, like the pharyngeal jaw in cichlid fishes, may be key to a group's success when they relax constraints on diversification by increasing phenotypic modularity. In cichlid fishes, pharyngeal jaw modifications that enhanced the ability to breakdown prey may have freed their oral jaws from serving their ancestral dual role as a site of both prey capture and prey processing. This functional decoupling that allowed the oral jaws to become devoted solely to prey capture has been hypothesized to have permitted the two sets of cichlid jaws to evolve independently. We tested the hypothesis that oral and pharyngeal jaw mechanics are evolutionarily decoupled both within and among Neotropical Heroine cichlids. In the trophically polymorphic species Herichthys minckleyi, molariforms that exhibit enlarged molarlike pharyngeal jaw teeth were found to have approximately 400% greater lower jaw mass compared to H. minckleyi with the alternative papilliform pharyngeal morphology. However, oral jaw gape, lower jaw velocity ratios, anterior jaw linkage mechanics, and jaw protrusion did not differ between the morphotypes. In 40 other Heroine species, there was a weak correlation between oral jaw mechanics and pharyngeal jaw mass when phylogenetic history was ignored. Yet, after expansion of the cytochrome b phylogeny for Heroines, change in oral jaw mechanics was found to be independent of evolutionary change in pharyngeal jaw mass based on independent contrasts. Evolutionary decoupling of oral and pharyngeal jaw mechanics has likely played a critical role in the unparalleled trophic diversification of cichlid fishes.     

Morphological variability in the Cuatro Cienegas cichlid, Cichlasoma minckleyi

The endemic cichlids of the Cuatro Cienegas Basin, Coahuila, Mexico are currently grouped in a single polymorphic species, Cichlasoma minckleyi . Two morphs of C. minckleyi were distinguished largely by features of the trophic apparatus, especially the pharyngeal dentition. Variation in body shape, based upon analysis of a set of linear measures, was continuous and did not allow recognition of discrete morphs. Individuals raised in the laboratory on several different diets indicated that trophic morphology had an important genetic component. Individuals raised in the laboratory, however, did not differentiate to the degree seen in comparably sized individuals collected at Cuatro Cienegas. This may be because snails used as food in the experiments were not as hard as endemic snails and indicated that some aspects of trophic morphology were also dependent upon environmental cues.     

Convergence in a mechanically complex phenotype: detecting structural adaptations for crushing in cichlid fish

Morphological convergence provides strong evidence that evolution is adaptive. However, putatively convergent morphology is often examined in two dimensions with no explicit model of function. In this study, we investigated structural and mechanical similarities of the lower pharyngeal jaw (LPJ) in cichlid fish that have evolved the ability to crush hard-shelled molluscs. Using a novel phylogeny, we demonstrated molluscivory has been gained and/or been lost numerous times in Heroine cichlids. Within this comparative framework, we produced three-dimensional computed tomography (CT) scans for LPJs of both morphotypes in the trophically polymorphic Herichthys minckleyi and six evolutionarily independent pairs of closely related species. Like H. minckleyi , these species exhibit divergence between a molluscivore and a nonmolluscivore. Using the CT scans, we generated finite element models of papilliform H. minckleyi LPJs to determine where stress would concentrate in a jaw not modified to crush molluscs. Then, we examined whether stress in the papilliform LPJ predicted structural modifications in molariform H. minckleyi and other molluscivorous species. Despite potential constraints, stresses imposed during prey processing explain 40% of LPJ variation in mollusc crushing species. The structural and mechanical analyses also suggest divergence found in polymorphic species could provide the substrate for trophic differences found in reproductively isolated cichlids.     

Influence of previous experience on the mate selection of two colour morphs of the convict cichlid, Cichlasoma nigrofasciatum (Pisces,Cichlidae)

In a pilot test, individuals of two colour morphs of Cichlasoma nigrofasciatum showed colour preferences in their schooling behaviour according to previous experience. Two further experiments were undertaken to investigate if such experientially induced preferences could reflect on the choice of mate. In one experiment white males who had been reared differently with regard to the colour morph of parents and siblings were given females of the different colour morphs (white and normal) to choose from, the females being successively removed after pairing to induce further choices. In this test, however, the males predominantly chose normal females, probably because of dominance relationships among the females, which masked a possible colour preference. Instead, a free choice test was devised, where 74 white and 74 normal fishes were allowed to pair off freely in a large tank. Here, a statistically significant sexual preference for the previously experienced colour morph was found. These results, as well as the possible evolutionary consequences, are discussed.     

Colour and levels of aggression in the midas cichlid

Previous work established that gold morphs of the Midas cichlid (Cichlasoma citrinellum) dominate normal ones of about the same size. Left unresolved, however, was whether the gold morphs dominate because they are inherently more aggressive or because the gold colour inhibits aggression. The issue was clarified here by comparing levels of aggression within groups of golds only, normals only, and golds plus normals. At first the groups of golds were the least aggressive. But 2 days later the levels of aggression in the other groups fell to about that of the golds. We conclude therefore that the gold colour inhibits attack, but that this effect is only discernible in groups when they are establishing inter-individual relationships disappearing when the groups stabilize. We suggest that gold coloration inhibits attacking by stimulating fear responses.     

Diet and morphology through ontogeny of the nonindigenous Mayan cichlid ‘<Emphasis Type="Italic">Cichlasoma</Emphasis> (<Emphasis Type="Italic">Nandopsis</Emphasis>)’ <Emphasis Type="Italic">urophthalmus</Emphasis> (Günther 1862) in southern Florida

We evaluated diet and morphology through ontogeny for a freshwater population of the Mayan cichlid Cichlasoma (Nandopsis) urophthalmus (Günther 1862) in Floridas Big Cypress National Preserve. This species is a generalist predator throughout ontogeny. Fish remained the primary prey item throughout ontogeny, but there was a shift from detritus and ostracods among juveniles to algae, gastropods (snails), decapods, Hymenoptera, and adult Diptera among adults. All morphological variables grew isometrically except total molariform tooth area and pharyngeal jaw mass, which exhibited positive allometry. Despite a moderately robust adult pharyngeal jaw apparatus, this species does not specialize on hard prey at this south Florida site. Compared to its native range in Mexico, fish in Florida have undergone a pronounced niche shift with the diet being dominated by fish and snails, probably due to greater availability. The invasive success of C. urophthalmus does not appear to be related to ontogenetic morphological shifts or dietary specialization. Rather, its successful and rapid colonization of southern Florida might in part be related to its generalized and opportunistic feeding habits and morphology.     

Variable discrimination and asymmetric preferences in laboratory tests of reproductive isolation between cichlid colour morphs

Mating behaviour affects reproductive isolation and phenotypic differentiation. In Lake Tanganyika, the cichlid fish Tropheus moorii diversified into numerous, currently allopatric colour variants. Allopatric isolation is periodically interrupted by dispersal and secondary contact during lake level fluctuations, making long‐term differentiation partly dependent on assortative mating. Laboratory experiments with two moderately distinct morphs revealed assortative female preferences in one (Nakaku), but random mate choice in the other morph (Mbita). No discrimination was apparent between two subtly differentiated morphs (Chimba and Moliro). Tested against each other in a previous study, the highly distinct Moliro and Nakaku exhibited strong assortative preferences. The correlation between colour pattern similarity and mate discrimination suggests that allopatry and philopatric behaviour are less crucial for the maintenance of differentiation between highly distinct morphs than for more similar morphs. Interestingly, the asymmetric isolation in one pair of morphs is congruent with a pattern of unidirectional mitochondrial introgression between populations.     

Buoyancy studies of three morphs of the Antarctic fish Trematomus newnesi (Nototheniidae) from the South Shetland Islands

Phenotypic plasticity, a widespread phenomenon in boreal freshwater fishes, is less apparent in the marine realm and the organism–environment interactions producing this variation are undetermined. A sample of 40 specimens of Trematomus newnesi, an inshore Antarctic fish from King George/25 de Mayo Island in the South Shetlands, was composed of 52.5% typical morphs, 27.5% large-mouth morphs and 20% intermediate morphs. Measurements of percentage buoyancy on the morphs of this sample were 3.73, 3.84 and 3.83%, respectively with no significant differences among means. Both mean dry skeletal weight as a percentage of body weight and mean oral jaw weight as a percentage of dry skeletal weight were significantly greater in large-mouth morphs compared to typical morphs. Diversification in head and jaw morphology is not accompanied by diversification in ecology as represented by buoyancy and, in spite of external appearances, measurements of buoyancy offer no support for the hypothesis that the large-mouth morph is more benthic than the typical semipelagic morph. Although a trophic basis for this polymorphism is possible, it has not yet been documented. Our discussion centers on the status of key open questions regarding morphism and highlights areas requiring more research.     

Colour biases in territorial aggression in a Neotropical cichlid fish

Discrete colour morphs have provided important insights into the evolution of phenotypic diversity. One of the mechanisms that can help to explain coexistence of ecologically similar colour morphs and incipient species is (colour) biased aggression, which has the potential to promote continued existence of the morphs in a frequency-dependent manner. I addressed colour biases in territorial aggression in a field-based study on a Neotropical cichlid fish species, Amphilophus sagittae, which has two ecologically indistinguishable colour morphs that mate assortatively. I found that A. sagittae, in particular females, were more aggressive towards models of their own colour than those mimicking colours of the other morph. Such a behavioural pattern should result in a selection regime that benefits the rarer morph, and hence could help explain how novel, rare phenotypes may avoid competitive exclusion.     

Where Am I? Niche constraints due to morphological specialization in two Tanganyikan cichlid fish species

Food resource specialization within novel environments is considered a common axis of diversification in adaptive radiations. Feeding specializations are often coupled with striking morphological adaptations and exemplify the relation between morphology and diet (phenotype–environment correlations), as seen in, for example, Darwin finches, Hawaiian spiders, and the cichlid fish radiations in East African lakes. The cichlids' potential to rapidly exploit and occupy a variety of different habitats has previously been attributed to the variability and adaptability of their trophic structures including the pharyngeal jaw apparatus. Here we report a reciprocal transplant experiment designed to explore the adaptability of the trophic structures in highly specialized cichlid fish species. More specifically, we forced two common but ecologically distinct cichlid species from Lake Tanganyika, Tropheus moorii (rock‐dweller), and Xenotilapia boulengeri (sand‐dweller), to live on their preferred as well as on an unpreferred habitat (sand and rock, respectively). We measured their overall performance on the different habitat types and explored whether adaptive phenotypic plasticity is involved in adaptation. We found that, while habitat had no effect on the performance of X. boulengeri, T. moorii performed significantly better in its preferred habitat. Despite an experimental duration of several months, we did not find a shift in the morphology of the lower pharyngeal jaw bone that would be indicative of adaptive phenotypic plasticity in this trait.     

Differential predation on colour morphs of the Midas cichlid, Cichlasoma citrinellum

Predation has often been invoked as a selective agent affecting colour patterns in a wide range of organisms, but data relating susceptibility to predation and objective measures of conspicuousness are rare. To investigate relative crypticity in free-swimming fishes, two colour morphs of the Midas cichlid were exposed to predation by largemouth bass, Micropterus salmoides. The two colour morphs, normal and amelanic golds, were viewed by predators in ponds against a uniform, natural background. Swimming pools, 4 m in diameter, were stocked with equal numbers of gold and normal juvenile Midas cichlids. Bass took a significantly higher proportion of normal-coloured fishes (69·2% of fish) than gold morphs overall, and in a significantly higher proportion of trials (68·8% of experiments). No differences were found between colour morphs in their behaviour or in the willingness of bass to attack either morph. The significance of these results are discussed in relation to the visual system of the predator and the relative conspicuousness of the prey colour patterns.     

Functional changes in the anatomy of the pharyngeal jaw apparatus of Astatoreochromis alluaudi (Pisces, Cichlidae), and their effects on adjacent structures

Organisms are tightly packed with structures so architectonic interdependency of structures is an obvious aspect of integration. This aspect of functional morphology, however, has received remarkably little attention. The present paper presents an example of the spatial relations among several apparatuses in the head of the cichlid fish, Astatoreochromis alluaudi. It investigates the transformations of these apparatuses and their functions due to a change in the pharyngeal jaw apparatus resulting from a functional shift (insect eating to snail crushing or vice versa ). The volume of the pharyngeal jaw apparatus differs 55% between the insect eating- and the snail eating morph. The increase in volume of the pharyngeal jaw apparatus has an impressive number of spatial effects, both direct and indirect, on other structures. Reallocation of space within the pharyngeal jaw apparatus occurs. Total head volume increases 31% but a reallocation of space is still necessary as the increase of the opercular compartment where the pharyngeal jaw apparatus is situated compensates for only 59% of the volume increase of that. Not all spatial effects do impose constraints. Spatial constraints are avoided when one of the apparatuses can use a topographically different volume of space. The respiratory apparatus shows internal reallocations of space without loss of total volume. The same solution occurs for elements of the expansion apparatus and the buccal savity. The eyes are not influenced. Finally spatial effects can have positive repercussions. The muscles of the oral jaw apparatus increase in size. This may be an example of an epiphenomenon.     

Sexual dimorphism in a trophically polymorphic cichlid fish?

Sexual dimorphism in ecologically relevant traits is ubiquitous in animals. However, other types of intraspecific phenotypic divergence, such as trophic polymorphism, are less common. Because linkage to sex should often lead to balancing selection, understanding the association between sex and phenotypic divergence could help explain why particular species show high morphological variability. To determine if sexual dimorphism could be helping to maintain ecomorphological variation in a classic case of intraspecific trophic polymorphism, we examined the association between sex and morphological divergence in the cichlid Herichthys minckleyi. Although H. minckleyi with enlarged molariform teeth on their pharyngeal jaws have been reported to more commonly be male, we did not find an association between sex and pharyngeal morphotype. Sex was associated with divergence in body size (as measured through standard length). But, sex was not associated with any of the other trophic traits examined. However, pharyngeal morphotype did show an association with gut length, gape, and tooth number. Sexual dimorphism is not playing a central role in enhancing trophic diversity within H. minckleyi. J. Morphol. 276:1448–1454, 2015. © 2015 Wiley Periodicals, Inc.     

Intrasexual competition among females and the stabilization of a conspicuous colour polymorphism in a Lake Victoria cichlid fish

The maintenance of colour polymorphisms within populations has been a long-standing interest in evolutionary ecology. African cichlid fish contain some of the most striking known cases of this phenomenon. Intrasexual selection can be negative frequency dependent when males bias aggression towards phenotypically similar rivals, stabilizing male colour polymorphisms. We propose that where females are territorial and competitive, aggression biases in females may also promote coexistence of female morphs. We studied a polymorphic population of the cichlid fish Neochromis omnicaeruleus from Lake Victoria, in which three distinct female colour morphs coexist: one plain brown and two blotched morphs. Using simulated intruder choice tests in the laboratory, we show that wild-caught females of each morph bias aggression towards females of their own morph, suggesting that females of all three morphs may have an advantage when their morph is locally the least abundant. This mechanism may contribute to the establishment and stabilization of colour polymorphisms. Next, by crossing the morphs, we generated sisters belonging to different colour morphs. We find no sign of aggression bias in these sisters, making pleiotropy unlikely to explain the association between colour and aggression bias in wild fish, which is maintained in the face of gene flow. We conclude that female-female aggression may be one important force for stabilizing colour polymorphism in cichlid fish.     

The Influence of Parental Color Morph on Mate Choice in the Cichlid Fish Cichlasoma nigrofasciatum

Cichlasoma nigrofasciatum of two different color morphs (striped or white), each of which had been taken care of from spawning up to 7 weeks of age by foster parents of the other color morph, were put together in a “free choice situation” and tested for their preference to spawn with a mate of the striped or of the white morph. The number of pairs of the same color (striped × striped, white × white) and of different color (“mixed” pairs, striped × white) was recorded and compared with the results of control fish. The latter had been taken care of from spawning up to 7 weeks of age by foster parents of the same color morph and were also tested in a free choice situation. The influence of parental color morph on mate choice was analysed in the first mate choice of naive animals (breeding for the first time). The stability over time of the preferences observed in the naive animals was then studied in the 18 months following the first mate choice experiment. Our results show that if young Cichlasoma nigrofasciatum had been taken care of by foster parents of the other color morph, but had grown up with siblings of their own color morph, approximately 9 % of the matings involved partners which had a different color (mixed pairs). In contrast, young which had been taken care of by foster parents of their own color morph and had grown up with siblings of their own color were completely segregated according to color during breeding (striped pairs or white pairs) and never formed mixed pairs. The importance of the influence of parental and sibling color morph on the preference to mate with a particular morph and, consequently, on speciation in cichlids in general are discussed.     

Functional morphology of durophagy in black carp,Mylopharyngodon piceus

The black carp, Mylopharyngodon piceus (Osteichthyes: Cyprinidae), crushes its snail and other molluscan prey with robust pharyngeal jaws and strong bite forces. Using gross morphology, histological sectioning, and X‐ray reconstruction of moving morphology (XROMM), we investigated structural, behavioral, and mechanical aspects of pharyngeal jaw function in black carp. Strut‐like trabeculae in their pharyngeal jaws support large, molariform teeth. The teeth occlude with a hypertrophied basioccipital process that is also reinforced with stout trabeculae. A keratinous chewing pad is firmly connected to the basioccipital process by a series of small bony projections from the base of the pedestal. The pharyngeal jaws have no bony articulations with the skull, and their position is controlled by five paired muscles and one unpaired median muscle. Black carp can crush large molluscs, so we used XROMM to compare pharyngeal jaw postures as fish crushed ceramic tubes of increasing sizes. We found that black carp increase pharyngeal jaw gape primarily by ventral translation of the jaws, with ventral rotation and lateral flaring of the jaws also increasing the space available to accommodate large prey items. A stout, robust ligament connects left and right jaws together firmly, but allows some rotation of the jaws relative to each other. Contrasting with the pharyngeal jaw mechanism of durophagous perciforms with fused left and right lower pharyngeal jaws, we hypothesize that this ligamentous connection may serve to decouple tensile and compressive forces, with the tensile forces borne by the ligament and the compressive forces transferred to the prey. J. Morphol. 276:1422–1432, 2015. © 2015 Wiley Periodicals, Inc.