Body size evolution of a shell‐brooding cichlid fish from Lake Tanganyika

The substrate‐brooding cichlid fish Telmatochromis temporalis in Lake Tanganyika demonstrates a simple example of ecological speciation between normal and dwarf morphs through divergent natural selection on body size. The dwarf morph most likely evolved from the ancestral normal morph; therefore, elucidating the evolution of its small body size is a key to understanding this ecological speciation event. Previous studies suggest that the small body size of the dwarf morph is an adaptation to the use of empty snail shells as shelters (males) and spawning sites (females), but this idea has not been fully evaluated. Combining original and previously published information, this study compared likelihood values to determine the primary factor that would be responsible for regulating the body size of the dwarf morph. Male body size is most likely regulated by the ability to turn within shells, which may influence the predation avoidance of adult fish. Females are smaller than males, and their body size is most likely regulated by the ability to lay eggs in the small spaces within shells close to the shell apices where predation risk on eggs is lower. This study provides new evidence supporting the hypothesis that different natural selection factors affected body size of the different sexes of the dwarf morph, which has not been reported in other animal species.     

Evidence for divergent natural selection of a Lake Tanganyika cichlid inferred from repeated radiations in body size

Divergent natural selection is thought to play a vital role in speciation, but clear, measurable examples from nature are still few. Among the many possible sources of divergent natural selection, predation pressure may be important because predators are ubiquitous in food webs. Here, we show evidence for divergent natural selection in a Lake Tanganyika cichlid, Telmatochromis temporalis , which uses burrows under stones or empty snail shells as shelters. This species contains normal and dwarf morphs at several localities. The normal morph inhabits rocky shorelines, whereas the dwarf morph invariably inhabits shell beds, where empty snail shells densely cover the lake bottom. Genetic evidence suggested that the dwarf morph evolved independently from the normal morph at two areas, and morphological analysis and evaluation of habitat structure revealed that the body sizes of morphs closely matched the available shelter sizes in their habitats. These findings suggest that the two morphs repeatedly evolved through divergent natural selection associated with the strategy for sheltering from predators.     

Environmental drivers of nematode abundance and genus composition at two spatial scales on an estuarine intertidal flat

Hydrobiologia - The dwarf morph of Telmatochromis temporalis uses empty snail shells as shelters and spawning sites. This morph varies in body colour from pale to dark within populations. Pale...     

A new morph of Telmatochromis temporalis (Cichlidae; Cichliformes) from Lake Tanganyika

Telmatochromis temporalis is a cichlid fish endemic to Lake Tanganyika. Two morphs of this species, normal and dwarf, form a good model for the study of ecological speciation through divergent natural selection on body size. This study reports a third morph of this species, slender morph, which was collected from deep waters off Kasenga, Zambia, whereas the normal morph inhabits shallow waters of the same locality. This study examined morphological characters and mitochondrial DNA sequences in 18 populations of the three T. temporalis morphs and two closely related species. The slender morph was morphologically similar to the normal and dwarf morphs of the same species, but clearly differed from closely related species. Genetic analyses showed that the slender morph was closest to but significantly different from the parapatric normal morph, suggesting reproductive isolation between them. Due to the lack of colour differences between morphs and of obvious geographical barriers between habitats, reproductive isolation between these morphs may be attributed to ecological factors, rather than sexual or geographical segregation. Further studies examining the evolution of the slender morph may deepen our knowledge of initial stages of speciation, like in the dwarf morph.

     

Alloparental care between catfishes in Lake Tanganyika

A bagrid catfish Auchenoglanis occidentalis cared for its brood, deposited within an accumulation of shells and gravel in the centre of a large saucer-like depression, for up to 2 weeks in Lake Tanganyika. Adults of another catfish Dinotopterus cunningtoni (Clariidae) persistently came to A. occidentalis nests near days of host spawning. Eggs of D. cunningtoni were found in the host nests on the day and within 2 days of host spawning. During and for a few days after the end of host brooding, associate species' young of much older ages than the host brood were often found in the nests together with those of a similar age to the host young. Associate young were rarely found in nests before spawning and in unused nests. These findings suggested that this brood-mixing has two origins: egg dumping by associate adults and voluntary intrusion of large associate young into host nests. Possible benefits to the associate species are to take advantage of nest preparation and parental behaviour of the host species and to feed on the host brood.     

Host nest defense against a color-dimorphic brood parasite: great reed warblers (Acrocephalus arundinaceus) versus common cuckoos (Cuculus canorus)

We tested great reed warbler (Acrocephalus arundinaceus) discrimination against two common cuckoo (Cuculus canorus) female color morphs (gray and rufous) in two areas with different parasitism rates and proportions of the two morphs. Hosts recognized the two cuckoo morphs from a control, the feral pigeon (Columba livia), at Apaj, Hungary (where brood parasitism was heavy), whereas no significant differences among the models were recorded at Lužice, Czech Republic (where the parasitism rate was moderate). At Apaj, the hosts discriminated the rufous morph (which is slightly predominant there) better than the gray morph from the control. Between-site comparison (after controlling for background aggression) revealed that great reed warblers were more aggressive towards the rufous morph at Apaj than at Lužice, whereas their responses to the gray morph did not differ, corresponding with much higher between-site difference in the relative abundance of the rufous morph. Our results suggest that both local parasitism pressure and relative abundance of two female color morphs of a brood parasite may significantly influence host nest defenses.     

Chitons’ apparent camouflage does not reduce predation by green crabs Carcinus maenas

Chitons are very common molluscs on European rocky shores. They are common prey of fish and crabs and often display several colour morphs within a given habitat. Predation is one of the potential mechanisms accounting for chiton colour polymorphism. The colour variation is considered to provide a camouflage protection through a match with the substratum surface typology. However, the effectiveness of chiton polymorphism as a predation defence requires further investigation. Previously we found a relationship between chiton colour morphs and substrate characteristics, with chitons most commonly found on substrates that were of similar colour to their shells. Here, we examined whether each morph displayed an active choice for matching the substratum. Next, we assessed if the predation success of the intertidal common crab Carcinus maenas varied significantly with the absence/presence of an apparent camouflage effect created between the chiton colour morph and the substratum type. The present study indicates that chiton colour morphs probably actively choose substratum types where they blend in. Carcinus maenas was able to prey on all Lepidochitona cinereus colour morphs, regardless of the substrate camouflage effect. Surprisingly, the predation frequency was higher on camouflaged chitons than on contrasting chitons. It was concluded that chiton camouflage is probably not a defence mechanism against predation by the crab C. maenas, and that chiton colour polymorphism is probably promoted by other, more visual predators.     

Intentional multiple mating by females in a species where sneak fertilization circumvents female choice for parental males

This paper describes how individual female ocellated wrasse Symphodus ocellatus distribute their spawning among males and nests in space and time. It is based on previously collected genetic data of larvae from ten different nests (used to reconstruct half and full‐sibling groupings both within and among nests on multiple days) and behavioural data of marked females across the reproductive season. Both the genetic analyses and behavioural observations confirm that female S. ocellatus intentionally engage in multiple mating, by repeatedly spawning at the same nest on different days and at several different nests (up to 12 spawning events over 3 weeks), leading to mixed paternity among her young. The main benefit of such high and intentional multiple mating is probably insurance against brood failure due to nest predation, desertion or poor paternal care by the male. These findings reveal that even in systems where females attempt to avoid male‐controlled mixed paternity, they may still engage in intentional multiple mating due to these potential benefits.     

Convergent evolutionary processes driven by foraging opportunity in two sympatric morph pairs of Arctic charr with contrasting post‐glacial origins

The expression of two or more discrete phenotypes amongst individuals within a species (morphs) provides multiple modes upon which selection can act semi‐independently, and thus may be an important stage in speciation. In the present study, we compared two sympatric morph systems aiming to address hypotheses related to their evolutionary origin. Arctic charr in sympatry in Loch Tay, Scotland, exhibit one of two discrete, alternative body size phenotypes at maturity (large or small body size). Arctic charr in Loch Awe segregate into two temporally segregated spawning groups (breeding in either spring or autumn). Mitochondrial DNA restriction fragment length polymorphism analysis showed that the morph pairs in both lakes comprise separate gene pools, although segregation of the Loch Awe morphs is more subtle than that of Loch Tay. We conclude that the Loch Awe morphs diverged in situ (within the lake), whereas Loch Tay morphs most likely arose through multiple invasions by different ancestral groups that segregated before post‐glacial invasion (i.e. in allopatry). Both morph pairs showed clear trophic segregation between planktonic and benthic resources (measured by stable isotope analysis) but this was significantly less distinct in Loch Tay than in Loch Awe. By contrast, both inter‐morph morphological and life‐history differences were more subtle in Loch Awe than in Loch Tay. The strong ecological but relatively weak morphological and life‐history divergence of the in situ derived morphs compared to morphs with allopatric origins indicates a strong link between early ecological and subsequent genetic divergence of sympatric origin emerging species pairs. The emergence of parallel specialisms despite distinct genetic origins of these morph pairs suggests that the effect of available foraging opportunities may be at least as important as genetic origin in structuring sympatric divergence in post‐glacial fishes with high levels of phenotypic plasticity. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Morphological divergence between three Arctic charr morphs – the significance of the deep‐water environment

Morphological divergence was evident among three sympatric morphs of Arctic charr (Salvelinus alpinus (L.)) that are ecologically diverged along the shallow‐, deep‐water resource axis in a subarctic postglacial lake (Norway). The two deep‐water (profundal) spawning morphs, a benthivore (PB‐morph) and a piscivore (PP‐morph), have evolved under identical abiotic conditions with constant low light and temperature levels in their deep‐water habitat, and were morphologically most similar. However, they differed in important head traits (e.g., eye and mouth size) related to their different diet specializations. The small‐sized PB‐morph had a paedomorphic appearance with a blunt head shape, large eyes, and a deep body shape adapted to their profundal lifestyle feeding on submerged benthos from soft, deep‐water sediments. The PP‐morph had a robust head, large mouth with numerous teeth, and an elongated body shape strongly related to their piscivorous behavior. The littoral spawning omnivore morph (LO‐morph) predominantly utilizes the shallow benthic–pelagic habitat and food resources. Compared to the deep‐water morphs, the LO‐morph had smaller head relative to body size. The LO‐morph exhibited traits typical for both shallow‐water benthic feeding (e.g., large body depths and small eyes) and planktivorous feeding in the pelagic habitat (e.g., streamlined body shape and small mouth). The development of morphological differences within the same deep‐water habitat for the PB‐ and PP‐morphs highlights the potential of biotic factors and ecological interactions to promote further divergence in the evolution of polymorphism in a tentative incipient speciation process. The diversity of deep‐water charr in this study represents a novelty in the Arctic charr polymorphism as a truly deep‐water piscivore morph has to our knowledge not been described elsewhere.     

Availability,uptake and regeneration of phosphate in mesocosms with varied levels of P deficiency

A population of cyclomorphic Bosmina coregoni was studied in Lake Östersjön, southwestern Sweden and results from field samples collected in 1988, 1989, 1990 and 1991 are presented. Animals collected in summer have remarkably higher carapace and prolonged antennule compared to what we call the normal morph. In 1991 the extreme morph reach its maximum body length, body height and antennule length in July to September. The occurrence of the extreme morph coincide with the hatching of the predaceous cladoceran Leptodora kindtii.The two morphs fluctuate in abundance and in relation to each other. In early spring only the normal morph occurred in the samples followed by a period of about two months when the two morphs were found together, in July only the extreme morph was found. In September the two morphs were again present in the lake. As has been shown for other cladoceran, the conspicuous carapace and antennule could be an adaptive response that decreases mortality due to invertebrate predation. Spectacular features like these are likely also accompanied by some sort of costs.     

Paternal inheritance of growth in fish pursuing alternative reproductive tactics

In species with indeterminate growth, age‐related size variation of reproductive competitors within each sex is often high. This selects for divergence in reproductive tactics of same‐sex competitors, particularly in males. Where alternative tactics are fixed for life, the causality of tactic choice is often unclear. In the African cichlid Lamprologus callipterus, large nest males collect and present empty snail shells to females that use these shells for egg deposition and brood care. Small dwarf males attempt to fertilize eggs by entering shells in which females are spawning. The bourgeois nest males exceed parasitic dwarf males in size by nearly two orders of magnitude, which is likely to result from greatly diverging growth patterns. Here, we ask whether growth patterns are heritable in this species, or whether and to which extent they are determined by environmental factors. Standardized breeding experiments using unrelated offspring and maternal half‐sibs revealed highly divergent growth patterns of male young sired by nest or dwarf males, whereas the growth of female offspring of both male types did not differ. As expected, food had a significant modifying effect on growth, but neither the quantity of breeding substrate in the environment nor ambient temperature affected growth. None of the environmental factors tested influenced the choice of male life histories. We conclude that in L. callipterus growth rates of bourgeois and parasitic males are paternally inherited, and that male and female growth is phenotypically plastic to only a small degree.     

The trade‐off between fecundity and egg size in a polymorphic population of Arctic charr (Salvelinus alpinus (L.)) in Skogsfjordvatn,subarctic Norway

Reproductive traits differ between intralacustrine Arctic charr morphs. Here, we examine three sympatric lacustrine Arctic charr morphs with respect to fecundity, egg size and spawning time/site to assess reproductive investments and trade‐offs, and possible fitness consequences. The littoral omnivore morph (LO‐morph) utilizes the upper water for feeding and reproduction and spawn early in October. The large profundal piscivore morph (PP‐morph) and the small profundal benthivore morph (PB‐morph) utilize the profundal habitat for feeding and reproduction and spawn in December and November, respectively. Females from all morphs were sampled for fecundity and egg‐size analysis. There were large differences between the morphs. The PB‐morph had the lowest fecundity (mean = 45, SD = 13) and smallest egg size (mean = 3.2 mm, SD = 0.32 mm). In contrast, the PP‐morph had the highest fecundity (mean = 859.5, SD = 462) and the largest egg size (mean = 4.5 mm, SD = 0.46 mm), whereas the LO‐morph had intermediate fecundity (mean = 580, SD = 225) and egg size (mean = 4.3, SD = 0.24 mm). Fecundity increased with increasing body size within each morph. This was not the case for egg size, which was independent of body sizes within morph. Different adaptations to feeding and habitat utilization have apparently led to a difference in the trade‐off between fecundity and egg size among the three different morphs.     

Patterns of morphological changes and hybridization between sympatric whitefish morphs (Coregonus spp.) in a Swiss lake: a role for eutrophication?

Whitefish, genus Coregonus, show exceptional levels of phenotypic diversity with sympatric morphs occurring in numerous postglacial lakes in the northern hemisphere. Here, we studied the effects of human‐induced eutrophication on sympatric whitefish morphs in the Swiss lake, Lake Thun. In particular, we addressed the questions whether eutrophication (i) induced hybridization between two ecologically divergent summer‐spawning morphs through a loss of environmental heterogeneity, and (ii) induced rapid adaptive morphological changes through changes in the food web structure. Genetic analysis based on 11 microsatellite loci of 282 spawners revealed that the pelagic and the benthic morph represent highly distinct gene pools occurring at different relative proportions on all seven known spawning sites. Gill raker counts, a highly heritable trait, showed nearly discrete distributions for the two morphs. Multilocus genotypes characteristic of the pelagic morph had more gill rakers than genotypes characteristic of benthic morph. Using Bayesian methods, we found indications of recent but limited introgressive hybridization. Comparisons with historical gill raker data yielded median evolutionary rates of 0.24 haldanes and median selection intensities of 0.27 for this trait in both morphs for 1948–2004 suggesting rapid evolution through directional selection at this trait. However, phenotypic plasticity as an alternative explanation for this phenotypic change cannot be discarded. We hypothesize that both the temporal shifts in mean gill raker counts and the recent hybridization reflect responses to changes in the trophic state of the lake induced by pollution in the 1960s, which created novel selection pressures with respect to feeding niches and spawning site preferences.     

Colour polymorphism in the intertidal snail Littorina rudis Maton

The tictors affecting the variation of shell colour morph frequencies of the intertidal snail Littorina rudis Maton have been examined using ordination and correlation techniques. The major gradient underlying variation in shell colour is related to habitat type and structure. Dark, patterned shells are characteristic of cliff and salt marsh habitats whilst light, unpatterned shells reach high frequencies on boulder shores. Colour morphs do not differ significantly in shell thickness and between-shore variation in colour morph frequencies cannot be directly attributed to habitat dilterences in the risk of shell injury, but to other factors associated with habitat type and structure, e.g. parasitism. It is suggested that the maintenance of shell colour polymorphism in L. rudis is probably mediated by selection on pleiotropic characters rather than shell colour alone.     

Geographic variation in Pemphigus populitransversus (Insecta: Aphididae)*†

The geographic variation of 33 morphological characters of two morphs of the gall-forming aphid Pemphigus populitransversus is studied in 214 locality samples. Among-locality variation ranges from 1 to 69% in the elongate morph and from 0 to 44% in the globular morph. The design of the study permits separation of interlocality correlations from intralocality correlations. The former are partly a function of the latter, confirming early observations on another Pemphigus species and on ticks. Factor analyses of both correlation matrices for both morphs yield four factors. Within localities these factors agree for the two morphs; among localities only one factor corresponds. Multiple discriminant analyses among localities of the two data sets do not correspond. There is little correlation between characters of stem mother and alate morphotypes within localities but such correlations are strong among localities. Maps are furnished for characters representing the independent dimensions of variation for each morph. Patterns of variation are shown to be significant by spatial autocorrelation analysis for both morphs but are much more marked in the elongate morph. Significant positive autocorrelation occurs up to 1000 km in the elongate morph – mostly only up to 200 km in the globular morph. There are two to three geographic variation patterns in the elongate morph, whereas in the globular morph the classes of patterns are less well defined and involve few characters. The environmental factors to which the globular and elongate morphs are adapting would appear to have different autocorrelation patterns. In each morph the patterns are clearly different and cannot be explained by a single microevolutionary process. The findings are compared with an earlier study in the related and largely sympatric P. populicaulis.     

Survival,behaviour and spatial distribution of shell morphs in a population of the snail Brephulopsis bidens (Pulmonata)

Summary Microspatial variation of banded and unbanded shell morphs frequencies as well as number of individuals per m², mortality, migration and burrowing into the ground were examined in a population of snail Brephulopsis bidens found in South Crimea mountains (USSR). Differential values of relative survival of morphs were determined by their thermotolerance. The relative survival of the banded morph was lower at the west sites of population area (W=0.273), and increased gradually up to 1 at the east sites. Survival of the banded morph was dependent on its burrowing activity. Differences in relative survival of morphs decreased parallel with increasing general mortality of snails.Burrowing activity and intensity of migration of the banded morph were significantly higher than that in unbanded. In experiments with artificial shaded sections, the banded morph preferred shaded sections, whereas unbanded chose illuminated sites. All these differences in behaviour probably form the main factors for microspatial variation of morph frequencies.     

EVIDENCE FOR BATESIAN MIMICRY IN A POLYMORPHIC HOVERFLY

Palatable Batesian mimics are avoided by predators because they resemble noxious or defended species. The striking resemblance of many hoverflies to noxious Hymenoptera is a “textbook” example of Batesian mimicry, but evidence that selection by predators has shaped the evolution of hoverfly patterns is weak. We looked for geographical and temporal trends in frequencies of morphs of the polymorphic hoverfly Volucella bombylans that would support the hypothesis that these morphs are Batesian mimics of different bumblebee species. The frequency of the black and yellow hoverfly morph was significantly positively related to the frequency of black and yellow bumblebees across 52 sites. Similarly, the frequency of the red‐tailed hoverfly morph was positively related to the frequency of red‐tailed bumblebees. However, the frequencies of hoverfly morphs were positively spatially autocorrelated, and after controlling for this, only one of the two common hoverfly morphs showed a significant positive relationship with its putative model. We conclude that the distribution of V. bombylans morphs probably reflects geographical variation in selection by predators resulting from differences in the frequencies of noxious bumblebee species.     

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.