PERMANENT GENETIC RESOURCES: Isolation and characterization of microsatellite loci in the cichlid fish in Lake Victoria, Haplochromis chilotes

Twelve short tandem repeat markers were successfully isolated from a cichlid, Haplochromis chilotes, in Lake Victoria, and characterized in Haplochromis pyrrhocephalus. The microsatellite regions of these markers were found to have between two and 48 alleles with heterozygosity ranging from 0.07 to 0.97. No loci showed significant departures from the Hardy–Weinberg or linkage equilibrium after the Bonferroni correction (P > 0.05). Cross‐species amplification in other cichlids of Lake Victoria, Haplochromis laparogramma, Lithochromis rubripinnis, L. rufus and Haplochromis sp. ‘rockkribensis’, was successful.     

Growth of the teleost eye: novel solutions to complex constraints

Synopsis The cichlid fish, Haplochromis burtoni, is highly dependent on vision for survival in its natural habitat. As is true of most teleost fishes, the eyes continue to grow throughout life without any obvious changes in visual capability. In H. burtoni, for example, retinal area may increase by 27 × in just 6 months. During growth, there is no obvious change in the visual sensitivity, visual acuity or lens quality which must all be appropriate for the enlarging eye. This requires that during growth competing constraints be met. For example, to maintain visual acuity, the number of ganglion cells per visual angle subtended on the retina must remain the same as must the convergence ratio of the cones onto those ganglion cells. In contrast, to maintain visual sensitivity, the number of rod photoreceptors per unit retinal area must remain the same. These requirements are in conflict since a larger eye may preserve acuity with fewer cells per unit area in a larger retina. In addition, the lens properties must remain the same as the animal increases in size so that the image available is of similar quality throughout life. Experiments have been performed to reveal the adaptations during growth which allow the fish to preserve its image of the world throughout life.     

What big lips are good for: on the adaptive function of repeatedly evolved hypertrophied lips of cichlid fishes

Linking phenotypic traits to an adaptive ecological function is a major goal of evolutionary biology. However, this task is challenging and has been accomplished in only a handful of species and ecological model systems. The repeatedly evolved adaptive radiations of cichlid fishes are composed of an enormously diverse set of species that differ in trophic morphology, body shape, coloration, and behaviour. Ecological guilds of species with conspicuously hypertrophied lips have evolved in parallel in all major cichlid radiations and are characterized by large lips and pointed and narrow heads. In the present study, we experimentally tested the adaptive significance of this set of conspicuous traits by comparing the success of hypertrophied‐lipped and closely‐related thin‐lipped endemic Lake Victoria cichlids in a novel foraging assay. The hypertrophied‐lipped species (Haplochromis chilotes) was clearly more successful in exploiting food resources from narrow crevices and the observed difference in foraging success increased more at narrower angles. Furthermore, pronounced differences in exploratory behaviour between the species suggest that the evolution of hypertrophied‐lipped species involved the co‐evolution of a suite of traits that include foraging behaviour. The repeated evolution of hypertrophied‐lip morphology in conjunction with a narrow and pointed head shape in cichlids represents an evolutionary innovation that facilitates foraging in rocky crevices, thus allowing access to a novel niche. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 448–455.     

Comparative studies on the eye morphology of lungless salamanders,family Plethodontidae,and the effect of miniaturization

In seven species of lungless salamanders, family Plethodontidae, ranging from medium to very small in body size and from small to very large in cell size, the morphology of the eye and the retina were investigated. Haller's rule was only partially corroborated. While the smallest species had the relatively largest eyes, the largest two species, having the largest cells, showed the third and fourth largest eyes of the series. An effect of cell size was also found with regard to eye morphology. Small species with small cells as well as large species with large cells had relatively small retinae and relatively large lenses. In contrast, small eyes with relatively large cells had absolutely and relatively large retinae and relatively small lenses. The retinae of all investigated plethodontids showed a morphology typical for land vertebrates with two fiber and three nuclear layers. Rods, cones and double cones could clearly be distinguished. A fovea or area centralis was not found. Retina ganglion cell and photoreceptor counts show that the number of these elements was lower than in salamandrids. However, determination of the resolution power of miniaturized eyes based on morphological and behavioral data shows that this does not seem to constitute a functional disadvantage. The morphological and functional properties and constraints of eyes of miniaturized salamanders are discussed.     

The Ontogeny of Social Behavior and Body Coloration in the African Cichlid Fish Haplochromis burtoni

The ontogeny of behavioral patterns and body coloration are described for the African cichlid fish, Haplochromis burtoni. The development of particular color patterns correlates directly with appearance of behavioral patterns which “use” those color patterns. There is a flexible timetable associated with these events which depends on both social and environmental factors.     

Size matters,but so does shape: quantifying complex shape changes in a sexually selected trait in stalk‐eyed flies (Diptera: Diopsidae)

The elaborate morphologies of sexually selected ornaments are ubiquitous across the animal kingdom. In studies investigating these traits, ornament size is frequently the focus, and empirical evidence supports its positive correlation with fitness. Yet shape plays an important role and, surprisingly, is often overlooked. Shape frequently changes with size, influenced by biomechanical, developmental, or performance constraints. Therefore, shape can provide additional insights into the morphological differences between individuals and the potential limits on sexual trait exaggeration. Here, we used landmark‐based geometric morphometric methods on a sexually dimorphic species of stalk‐eyed fly (Teleopsis dalmanni) to examine patterns of sexual shape dimorphism. Our analyses reveal a significant difference in head shape between the sexes, with males exhibiting smaller eye bulbs, thinner stalks, and smaller heads than females. Additionally, as eyestalk length increases within each sex, a similar pattern of shape change was observed as that observed between sexes. This pattern of shape change may be the result of constraints acting against further ornament exaggeration, and we suggest that this may significantly impact the whole‐organism performance in stalk‐eyed flies. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 104–113.     

Functional morphology of the visual system and mating strategies in bumblebees (Hymenoptera,Apidae, Bombus)

Bumblebee mating behaviour intrigued Darwin over 150 years ago and has elicited much interest since. Despite our increasing knowledge about male mating strategies, we still know little about the signals and cues involved, the sender‐receiver relationship and the functional adaptations of the involved sensory systems. Although several authors have noticed a close relationship between the mating system and male‐specific elaboration of the visual system, studies on the functional adaptations have yet to be conducted. We investigated the functional morphology of the compound eyes in 11 species of Bombus from various subgenera in detail. Of these, four species (Bombus confusus, Bombus melaleucus, Bombus mendax, Bombus niveatus) have enlarged male eyes, characterized by a higher number of ommatidia compared with worker eyes and a frontal zone with enlarged facets, which is likely to be associated with improved spatial resolution and contrast sensitivity. In these species, perching mating strategies are found. In contrast, males of species that patrol scent routes (Bombus hortorum, Bombus lapidarius, Bombus pascuorum, Bombus pratorum, Bombus soroeensis, Bombus terrestris, Bombus wurflenii) show no distinct eye adaptations, and their eye morphology closely resembles that of the workers. A phylogenetic analysis of male eye structure indicates that enlarged males eyes may have been the ancestral state in Bombus. © 2014 The Linnean Society of London     

Midwater spawning inHaplochromis chrysonotus (Boulenger) (Teleostei: Cichlidae) in Lake Malawi

Synopsis Haplochromis chrysonotus, a semipelagic shoaling cichlid from Lake Malawi, has been observed spawning in open water up to ten metres above the substratum. It is suggested that open water spawning without the establishment of a substratum-based territory eliminates competition with other species for breeding space and that it may be a stage in the evolution of a totally pelagic mode of life.     

Adaptive responses in resurgent Lake Victoria cichlids over the past 30 years

Textbook examples of adaptive radiation like the Galapagos finches and the East-African cichlids form a subject of major interest in evolutionary biology. Many of these species often show rapid morphological changes in response to a perturbed environment. The dramatic ecological changes in Lake Victoria during the past three decades, e.g. Nile perch predation and eutrophication, provide a unique opportunity to study environmental effects on cichlid morphology. Preliminary research has revealed that the lake’s haplochromines tend to be extremely plastic and sensitive to these environmental changes. So far, long-term ecomorphological studies at short-term intervals are extremely rare. In this study, we examined morphological changes over a 30 year period in six haplochromine species. Geometric morphometric analyses at intervals of approximately 3 years revealed adaptive responses. Three out of four resurgent haplochromines had a smaller head surface/caudal peduncle area (HS/CPA) ratio during the upsurge of the predatory Nile perch. During the same period, all four resurgent species had a larger cheek depth and a smaller eye size. The smaller HS/CPA ratio and larger cheek depth are likely to be adaptive responses to a high predation pressure and a diet shift to larger prey. The smaller eye size seems to be the result of a trade off between the eyes and other morphological structures in the smaller head of these species. Interestingly, the direction of the morphological changes was different between the four resurgent cichlid species and two species that became extremely rare or even may have gone extinct. The HS/CPA ratio increased in the extinct species where it decreased in the resurgent species. This study suggests that predation is a major driver of these morphological changes, which may be due to either phenotypic plasticity or adaptive changes.     

Comparative retinal anatomy in four species of elasmobranch

Using both light and transmission electron microscopy, we examined the retinal anatomy of four elasmobranch species with differing ecologies: the bull shark Carcharhinus leucas, Port Jackson shark Heterodontus portusjacksoni, epaulette shark Hemiscyllium ocellatum and pink whipray Himantura fai. Their retinas are typical of other vertebrates, having three nuclear and two synaptic layers, but are characterised by very large horizontal cells, low densities of ganglion cells (many of which are displaced to the inner nuclear and inner plexiform layers) and the presence of numerous myelinated axons within the nerve fibre layer. Carcharhinus leucas, H. fai and H. ocellatum have duplex retinas containing both rods and single cones. The peak ratio of rods to cones is much lower in C. leucas (4:1) and H. fai (3:1) compared to H. ocellatum (19:1), reflecting differences in diel activity patterns. No cones were observed in the retina of H. portusjacksoni, which is strongly nocturnal. The cones of H. fai lack a distinct myoid and their nuclei are located in a discrete layer sclerad to the external limiting membrane (ELM), whereas those of C. leucas and H. ocellatum have an obvious myoid, and their nuclei are located vitread to the ELM. No double/twin cones were observed in any species. Incorporating data from other studies, there is a clear correlation between rod outer segment volume and visual ecology in elasmobranchs, with smaller volumes found in partly diurnal pelagic species and larger volumes in benthic nocturnal species. This trend may reflect fundamental differences in visual temporal resolution between active and more sedentary species. J. Morphol., 2012. © 2011 Wiley Periodicals, Inc.     

Photoreceptors and eyes of pikeperch Sander lucioperca,pike Esox lucius,perch Perca fluviatilis and roach Rutilus rutilus from a clear and a brown lake

The photoreceptors and eyes of four fish species commonly cohabiting Fennoscandian lakes with different light transmission properties were compared: pikeperch Sander lucioperca, pike Esox lucius, perch Perca fluviatilis and roach Rutilus rutilus. Each species was represented by individuals from a clear (greenish) and a humic (dark brown) lake in southern Finland: Lake Vesijärvi (LV; peak transmission around 570 nm) and Lake Tuusulanjärvi (LT; peak transmission around 630 nm). In the autumn, all species had almost purely A2-based visual pigments. Rod absorption spectra peaked at c.526 nm (S. lucioperca), c. 533 nm (E. lucius) and c. 540 nm (P. fluviatilis and R. rutilus), with no differences between the lakes. Esox lucius rods had remarkably long outer segments, 1.5–2.8-fold longer than those of the other species. All species possessed middle-wavelength-sensitive (MWS) and long-wavelength-sensitive (LWS) cone pigments in single, twin or double cones. Rutilus rutilus also had two types of short-wavelength sensitive (SWS) cones: UV-sensitive [SWS1] and blue-sensitive (SWS2) cones, although in the samples from LT no UV cones were found. No other within-species differences in photoreceptor cell complements, absorption spectra or morphologies were found between the lakes. However, E. lucius eyes had a significantly lower focal ratio in LT compared with LV, enhancing sensitivity at the expense of acuity in the dark-brown lake. Comparing species, S. lucioperca was estimated to have the highest visual sensitivity, at least two times higher than similar-sized E. lucius, thanks to the large relative size of the eye (pupil) and the presence of a reflecting tapetum behind the retina. High absolute sensitivity will give a competitive edge also in terms of short reaction times and long visual range.     

Major morphological changes in a Lake Victoria cichlid fish within two decades

During the upsurge of the introduced predatory Nile perch in Lake Victoria in the 1980s, the zooplanktivorous Haplochromis ( Yssichromis ) pyrrhocephalus nearly vanished. The species recovered coincident with the intense fishing of Nile perch in the 1990s, when water clarity and dissolved oxygen levels had decreased dramatically due to increased eutrophication. In response to the hypoxic conditions, total gill surface in resurgent H. pyrrhocephalus increased by 64%. Remarkably, head length, eye length, and head volume decreased in size, whereas cheek depth increased. Reductions in eye size and depth of the rostral part of the musculus sternohyoideus, and reallocation of space between the opercular and suspensorial compartments of the head may have permitted accommodation of larger gills in a smaller head. By contrast, the musculus levator posterior, located dorsal to the gills, increased in depth. This probably reflects an adaptive response to the larger and tougher prey types in the diet of resurgent H. pyrrhocephalus . These striking morphological changes over a time span of only two decades could be the combined result of phenotypic plasticity and genetic change and may have fostered recovery of this species.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 41–52.     

Evolution of the third eye: a phylogenetic comparative study of parietal‐eye size as an ecophysiological adaptation in Liolaemus lizards

The parietal, or third, eye is a photosensory organ situated in the middle of the skull of many lizards. Despite many hypotheses, its exact ecological functions are still unclear. Studies have compared the presence and absence of a functioning parietal eye, although there are no quantitative studies of parietal‐eye traits in relation to ecology, physiology or behaviour. In the present study, we report the first comparative study of relative parietal‐eye size in relation to climatic and thermophysiological variables. We studied thirty species of Liolaemus, a genus of South‐American lizards inhabiting a range of climatic conditions, but found little evidence for adaptation to thermal environment, in that parietal‐eye size did not vary meaningfully with latitude, altitude or any measures of environmental temperature. Neither did it relate to thermophysiology; there was a weak relation to thermal tolerance, although this was partially confounded with body size, which explained 23% of the among‐species variance after controlling for within‐species variation. The negative results obtained could not be explained by phylogenetic constraints because we found no evidence of phylogenetic inertia. We also observed high intraspecific variation indicating that parietal‐eye size may not be under strong selection for accuracy. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 870–883.     

The roles of pre‐ and post‐hatching growth rates in generating a latitudinal cline of body size in the eastern fence lizard (Sceloporus undulatus)

Countergradient variation in norms of reaction can dampen the direct effects of environmental influences on phenotypic traits, allowing phenotypic similarity among populations despite exposure to different environmental conditions. Such norms of reaction may occur at any phase of the life‐history (e.g. growth rates during both embryonic and postembryonic stages may influence geographical variation in adult body size). We collected gravid female lizards (Sceloporus undulatus) from northern (Indiana), central (Mississippi), and southern (Florida) populations, spanning almost the full latitudinal range of the species. Adult females from the southern population were smaller. Intrinsic growth rates of hatchlings were higher for the central population than for the other two populations. This pattern does not parallel the countergradient variation previously found in embryonic developmental rates among these populations. Earlier hatching enhanced survival rates of juveniles to a similar degree among populations, although juvenile survival rates in the field generally increase with latitude in this species. Our data reveal geographical variation in the ways in which intrinsic developmental/growth rates and survival shift during ontogeny, and suggest that latitudinal patterns in adult body size (such as Bergmann's rule) can result from both faster growth, and longer periods of growth. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 202–209.     

Wing shape,wing size,and sexual dimorphism in eye‐span in stalk‐eyed flies (Diopsidae)

The eyes of stalk‐eyed flies (Diopsidae) are positioned at the end of rigid peduncles (‘stalks’) protruding laterally from the head. Eye‐stalk length varies within the family and, in some species, varies between males and females. Larger eye‐stalks in males result from sexual selection for longer stalks, a trait that increases male reproductive success. In the present study, we examined whether an increase in eye‐stalk length results in an adjustment of wing size and shape to deal with the burden of bearing an exaggerated ‘ornament’. We compared wing morphology among ten species of stalk‐eyed flies that differ in eye‐span and the degree of sexual dimorphism. Mass‐specific wing length differed between males and females in seven out of the ten species. Nondimensional wing shape parameters differed between the species (P < 0.001), but mostly did not differ between males and females of the same species. Dimorphism in eye‐span closely correlated with dimorphism in wing length (r = 0.89, P < 0.001) and the correlation remained significant (r = 0.81, P = 0.006) after correcting for phylogenetic relationships. Once corrected for phylogenetic relatedness, the mass‐specific wing length of males (but not females) was weakly correlated with mass‐specific eye‐span (r = 0.66, P = 0.042). We propose that the observed proportional increase in wing length associated with increased eye‐span can facilitate aerial manoeuverability, which would otherwise be handicapped by the elevated moment of inertia imposed by the wider head. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 860–871.     

Correlating head shape with ecological variables in rock-dwelling haplochromines (Teleostei: Cichlidae) from Lake Victoria

An exploratory analysis was made of the head shape of cichlid fishes. A 3-D head truss was used, which allowed approximations of the volumes of three compartments of the head. We applied the method to six species of rock-dwelling haplochromine cichlids, of which we studied 12 populations from four rocky islands in the southern part of Lake Victoria. Head shape was correlated with eight environmental variables. Truss distances and compartment volumes correlated with these variables, e.g. volumes of the compartments containing the gills correlated (negatively) with oxygen levels; truss distances, including the oral jaws and their musculature, correlated with food composition; and eye size correlated with width of the transmission spectrum. Another finding was the likely architectonic interactions between anatomical elements. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 39–48.     

Female mating preferences and male coloration covary with water transparency in a Lake Victoria cichlid fish

Rapid speciation in Lake Victoria cichlid fish of the genus Pundamilia may be facilitated by sexual selection: female mate choice exerts sexual selection on male nuptial coloration within species and maintains reproductive isolation between species. However, declining water transparency coincides with increasingly dull coloration and increasing hybridization. In the present study, we investigated the mechanism underlying this pattern in Pundamilia nyererei, a species that interbreeds with a sister species in turbid but not in clear water. We compared measures of intraspecific sexual selection between two populations from locations that differ in water transparency. First, in laboratory mate‐choice experiments, conducted in clear water and under broad‐spectrum illumination, we found that females originating from turbid water have significantly weaker preferences for male coloration than females originating from clear water. Second, both the hue and body coverage of male coloration differ between populations, which is consistent with adaptation to different photic habitats. These findings suggest that the observed relationship between male coloration and water transparency is not mediated by environmental variation alone. Rather, female mating preferences are indicated to have changed in response to this variation, constituting the first evidence for intraspecific preference‐trait co‐evolution in cichlid fish. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 398–406.     

The effects of Acanthaster planci predation on populations of two species of massive coral

Species of the freshwater planarian genus Polycelis have a variable number of eyes in the head, typically more than a hundred. To elucidate the mechanisms determining the number of eyes, we investigated the relation between eye number and body length in Polycelis sapporo (Ijima & Kaburaki), a non-fissioning species, and P. auriculata Ijima & Kaburaki, a fissioning species. In P. sapporo reared at 7–8 °C, a positive correlation existed between number of eyes and body length. Eye number decreased with starvation. A similar correlation was true of P. auriculata. In specimens of P. auriculata undergoing regeneration, the rate of eye formation was higher in newly formed heads originating from larger tail-pieces than in those from smaller pieces. As a head regenerated from a tail piece or as the body size increased with feeding, the number of eyes increased. These results suggest that the number of eyes in an individual of Polycelis is determined by body length. The fine structure of the photoreceptor and pigment cells in the eyes of P. auriculata is similar to that of comparable cells in the pair of eyes in Dugesia despite the difference in the number of cells comprising an eye.     

Ecological constraints on sensory systems: compound eye size in Daphnia is reduced by resource limitation

Eye size is an indicator of visual capability, and macroevolutionary patterns reveal that taxa inhabiting dim environments have larger eyes than taxa from bright environments. This suggests that the light environment is a key driver of variation in eye size. Yet other factors not directly linked with visual tasks (i.e., non-sensory factors) may influence eye size. We sought to jointly investigate the roles of sensory (light) and non-sensory factors (food) in determining eye size and ask whether non-sensory factors could constrain visual capabilities. We tested environmental influences on eye size in four species of the freshwater crustacean Daphnia, crossing bright and dim light levels with high and low resource levels. We measured absolute eye size and eye size relative to body size in early and late adulthood. In general, Daphnia reared on low resources had smaller eyes, both absolutely and relatively. In contrast to the dominant macroevolutionary pattern, phenotypic plasticity in response to light was rarely significant. These patterns of phenotypic plasticity were true for overall diameter of the eye and the diameter of individual facets. We conclude that non-sensory environmental factors can influence sensory systems, and in particular, that resource availability may be an important constraint on visual capability.     

Ecological preference between generalist and specialist rodents: spatial and environmental correlates of phenotypic variation

Different ecological preferences among species may result in differences in response to similar environmental variation. To test this hypothesis, we assessed the patterns of skull and mandible size and shape variation in three Sigmodontinae mice from agroecosystems of central Argentina with increasing degree of specialization: Calomys musculinus, Akodon azarae and Oxymycterus rufus. Spatial patterns in size and shape were analysed after controlling for allometry and sexual dimorphism using a total of 697 specimens. We then evaluated the covariation between shape, climatic and environmental variables and assessed the contribution of distinct climatic and environmental variables to phenotypic variability. Oxymycterus rufus displayed a marked spatial structure, and there was a high correlation between shape, climatic and environmental variables in this species. Climatic and environmental variables had a moderate effect on the phenotype of A. azarae, and were not correlated with morphological variation in C. musculinus. Our study highlights the difference in phenotypic responses to spatial and environmental gradients across coexisting species, specialist species displaying a more marked spatial structure in morphology than generalist species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 180–203.