Divergent ontogenies of trophic morphology in two closely related haplochromine cichlids

Fish develop morphological specializations in their trophic and locomotor systems as a result of varying functional demands in response to environmental pressures at different life stages. These specializations should maximize particular performances in specialists, adapting them to their trophic and habitat niches at each ontogenetic stage. Because differential growth rates of the structural components comprised in the head are likely to be linked to the diet of a fish throughout its development, we investigated the ontogenetic development of two haplochromine cichlid species belonging to different trophic guilds. We employed geometric morphometric techniques to evaluate whether starting from morphologically similar fry they diverge into phenotypes that characterize trophic guilds and locomotor types. Our examination of overall body shape shows that certain specialized morphological features are already present in fry, whereas other traits diverge through ontogeny due to differences in species‐specific allometric variation. Allometric shape variation was found to be more relevant for the biter specialist than for the sucker morphotype. Our results confirm that phenotypic changes during ontogeny can be linked to dietary and habitat shifts in these fish. Furthermore, evidence for an integrated development of trophic and locomotor specializations in morphology was observed. J. Morphol. 276:860–871, 2015. © 2015 Wiley Periodicals, Inc.     

Effects of habitat complexity,dominance and personality on habitat selection: Ideal despotic cichlids

Habitat structure can impede visibility and movement, resulting in lower resource monopolization and aggression. Consequently, dominant individuals may prefer open habitats to maximize resource gain, or complex habitats to minimize predation risk. We explored the role of dominance on foraging, aggression and habitat choice using convict cichlids (Amatitlania nigrofasciata) in a two‐patch ideal free distribution experiment. Groups of six fish of four distinct sizes first competed for shrimp in one‐patch trials in both an open and complex habitat; half the groups experienced each habitat type first. Following these one‐patch trials, each group then chose between habitat types in a two‐patch trial while competing for food. Finally, each fish underwent an individual behavioural assessment using a battery of “personality” tests to determine if behaviour when alone accurately reflected behaviour within a social context. In the one‐patch trials, dominant fish showed similar food consumption between habitats, but chased more in the complex habitat. In the two‐patch choice trials, dominants preferred and defended the complex habitat, forming an ideal despotic distribution with more than half the fish and competitive weight in the open habitat. Within the groups, individual fish differed in foraging and chasing, with repeatabilities of 0.45 and 0.23 across all treatments. Although a higher foraging rate during the individual assessment predicted foraging rate and use of the complex habitat during the group trials, aggression and boldness tests were not reflective of group behaviour. Across groups, heavier dominants and those with higher foraging rate in the open habitat used the open habitat more, suggesting that both risk and energetic state affect habitat preference in dominant convict cichlids.     

Resistance to change varies inversely with reinforcement context

We report two experiments which test whether resistance to prefeeding and satiation for a variable-interval (VI) schedule that delivers a constant rate of reinforcement varies inversely with the reinforcement rate for an alternative schedule. In Experiment 1, eight pigeons responded in a multiple schedule in which the red key was always associated with a VI 90-s schedule and the green key with either a richer (VI 18s) or leaner (VI 540s) schedule in different conditions. After baseline training in each condition, prefeeding test sessions were conducted in which 10g, 20g, 30g, 40g, and 50g food were provided one-hour prior to test. Additional baseline training was given between each test session. In Experiment 2, two groups of pigeons responded in a multiple schedule similar to Experiment 1. After baseline training, pigeons were exposed to a 5-h satiation test session in which the VI 90-s schedule was available continuously. Test sessions were conducted when pigeons were maintained at 85%, 95%, and 85% of their body weights in an ABA design. Results of both experiments showed that responding in the VI 90-s schedule that alternated with a leaner schedule during baseline was more resistant to prefeeding and satiation. These data rule out alternative explanations for results of previous studies, and confirm that resistance to change varies inversely with reinforcement context.     

Hybridization between closely related songbirds is related to human habitat disturbance

Human habitat disturbances can promote hybridization between closely related, but typically reproductively isolated, species. We explored whether human habitat disturbances are related to hybridization between two closely related songbirds, black-capped and mountain chickadees, using both genomic and citizen science data sets. First, we genotyped 409 individuals from across both species' ranges using reduced-representation genome sequencing and compared measures of genetic admixture to a composite measure of human landscape disturbance. Then, using eBird observations, we compared human landscape disturbance values for sites where phenotypically diagnosed hybrids were observed to locations where either parental species was observed to determine whether hybrid chickadees are reported in more disturbed areas. We found that hybridization between black-capped and mountain chickadees positively correlates with human habitat disturbances. From genomic data, we found that (1) hybrid index (HI) significantly increased with habitat disturbance, (2) more hybrids were sampled in disturbed habitats, (3) mean HIs were higher in disturbed habitats versus wild habitats, and (4) hybrids were detected in habitats with significantly higher disturbance values than parentals. Using eBird data, we found that both hybrid and black-capped chickadees were significantly more disturbance-associated than mountain chickadees. Surprisingly, we found that nearly every black-capped chickadee we sampled contained some proportion of hybrid ancestry, while we detected very few mountain chickadee backcrosses. Our results highlight that hybridization between black-capped and mountain chickadees is widespread, but initial hybridization is rare (few F1s were detected). We conclude that human habitat disturbances can erode pre-zygotic reproductive barriers between chickadees and that post-zygotic isolation is incomplete. Understanding what becomes of recently hybridizing species following large-scale habitat disturbances is a new, but pressing, consideration for successfully preserving genetic biodiversity in a rapidly changing world.     

Divergence with gene flow in the rock-dwelling cichlids of Lake Malawi

Within the past two million years, more than 450 species of haplochromine cichlids have diverged from a single common ancestor in Lake Malawi. Several factors have been implicated in the diversification of this monophyletic clade, including changes in lake level and low levels of gene flow across limited geographic scales. The objectives of this study were to determine the effect of recent lake-level fluctuations on patterns of allelic diversity in the genus Metriaclima, to describe the patterns of population structure within this genus, and to identify barriers to migration. This was accomplished through an analysis of allele frequencies at four microsatellite loci. Twelve populations spanning four species within Metriaclima were surveyed. The effect of lake-level fluctuations can be seen in the reduced genetic diversity of the most recently colonized sites; however, genetic diversity is not depressed at the species level. Low levels of population structure exist among populations, yet some gene flow persists across long stretches of inhospitable habitat. No general barrier to migration was identified. The results of this study are interpreted with respect to several speciation models. Divergence via population bottlenecks is unlikely due to the large allelic diversity observed within each species. Genetic drift and microallopatric divergence are also rejected because some gene flow does occur between adjacent populations. However, the reduced levels of gene flow between populations does suggest that minor changes in the selective environment could cause the divergence of populations.     

Body shape differences in a pair of closely related Malawi cichlids and their hybrids: Effects of genetic variation,phenotypic plasticity,and transgressive segregation

Phenotypic differences may have genetic and plastic components. Here, we investigated the contributions of both for differences in body shape in two species of Lake Malawi cichlids using wild‐caught specimens and a common garden experiment. We further hybridized the two species to investigate the mode of gene action influencing body shape differences and to examine the potential for transgressive segregation. We found that body shape differences between the two species observed in the field are maintained after more than 10 generations in a standardized environment. Nonetheless, both species experienced similar changes in the laboratory environment. Our hybrid cross experiment confirmed that substantial variation in body shape appears to be genetically determined. The data further suggest that the underlying mode of gene action is complex and cannot be explained by simple additive or additive‐dominance models. Transgressive phenotypes were found in the hybrid generations, as hybrids occupied significantly more morphospace than both parentals combined. Further, the body shapes of transgressive individuals resemble the body shapes observed in other Lake Malawi rock‐dwelling genera. Our findings indicate that body shape can respond to selection immediately, through plasticity, and over longer timescales through adaptation. In addition, our results suggest that hybridization may have played an important role in the diversification of Lake Malawi cichlids through creating new phenotypic variation.     

Seasonal changes in habitat preferences of two closely related millipede species

The habitat preferences of two closely related millipede species, Centrobolus richardii and C. fulgidus, were investigated on three different seral stages of a coastal dune forest successional sere north of Richards Bay, South Africa. Fixed‐width transects were used to survey millipedes in three habitats of different ages. Habitat preference occurred on both inter‐ and intra‐site levels and was influenced by season. A habitat shift was recorded for C. richardii, while C. fulgidus was dormant during the winter months, reflecting two different strategies used by these closely related species to meet their resource requirements. Successional changes previously reported are masked by these differential responses.     

Color patterns and species recognition in four closely related species of Lake Malawi cichlid

We examined interspecific female mating preferences in fourclosely related species of cichlid belonging to the Pseudotropheuszebra species complex of Lake Malawi. These species differin coloration but are similar in other respects, suggestingthat male color patterns may be important to female mate choicein species recognition. To test this hypothesis, we presented females from each species with a choice of four males, one ofher own species and three others that were each of a differentspecies. We also gave each female a choice between the threeheterospecific males only. In all four species, females showeda significant preference for conspecific males in the four-waychoice and chose the male with the most similar color patternto the conspecific male in the three-way choice. These resultsare discussed with reference to the theory of sexual selectionon color patterns as a means of sympatric speciation in cichlids.     

Geography disentangles introgression from ancestral polymorphism in Lake Malawi cichlids

Phenotypically diverse Lake Malawi cichlids exhibit similar genomes. The extensive sharing of genetic polymorphism among forms has both intrigued and frustrated biologists trying to understand the nature of diversity in this and other rapidly evolving systems. Shared polymorphism might result from hybridization and/or the retention of ancestrally polymorphic alleles. To examine these alternatives, we used new genomic tools to characterize genetic differentiation in widespread, geographically structured populations of Labeotropheus fuelleborni and Metriaclima zebra. These phenotypically distinct species share mitochondrial DNA (mtDNA) haplotypes and show greater mtDNA differentiation among localities than between species. However, Bayesian analysis of nuclear single nucleotide polymorphism (SNP) data revealed two distinct genetic clusters corresponding perfectly to morphologically diagnosed L. fuelleborni and M. zebra. This result is a function of the resolving power of the multi‐locus dataset, not a conflict between nuclear and mitochondrial partitions. Locus‐by‐locus analysis showed that mtDNA differentiation between species (F_CT) was nearly identical to the median single‐locus SNP F_CT. Finally, we asked whether there is evidence for gene flow at sites of co‐occurrence. We used simulations to generate a null distribution for the level of differentiation between co‐occurring populations of L. fuelleborni and M. zebra expected if there was no hybridization. The null hypothesis was rejected for the SNP data; populations that co‐occur at rock reef sites were slightly more similar than expected by chance, suggesting recent gene flow. The coupling of numerous independent markers with extensive geographic sampling and simulations utilized here provides a framework for assessing the prevalence of gene flow in recently diverged species.     

Plasticity of opsin gene expression in cichlids from Lake Malawi

Sensory systems play crucial roles in survival and reproduction. Therefore, sensory plasticity has important evolutionary implications. In this study, we examined retinal plasticity in five species of cichlid fish from Lake Malawi. We compared the cone opsin expression profiles of wild‐caught fish to lab‐reared F₁ that had been raised in a UV minus, reduced intensity light environment. All of the opsin genes that were expressed in wild‐caught fish were also expressed in lab‐reared individuals. However, we found statistically significant differences in relative opsin expression among all five species. The most consistent difference was in the SWS2B (violet) opsin, which was always expressed at higher levels in lab‐reared individuals. Estimates of visual pigment quantum catch suggest that this change in expression would increase retinal sensitivity in the light environment of the lab. We also found that the magnitude of plasticity varied across species. These findings have important implications for understanding the genetic regulation of opsin expression and raise many interesting questions about how the cichlid visual system develops. They also suggest that sensory plasticity may have facilitated the ecological diversification of cichlids in Lake Malawi.     

Axes of differentiation in the bower-building cichlids of Lake Malawi

The 500-1000 cichlid species endemic to Lake Malawi constitute one of the most rapid and extensive radiations of vertebrates known. There is a growing debate over the role natural and sexual selection have played in creating this remarkable assemblage of species. Phylogenetic analysis of the Lake Malawi species flock has been confounded by the lack of appropriate morphological characters and an exceptional rate of speciation, which has allowed ancestral molecular polymorphisms to persist within species. To overcome this problem we used amplified fragment length polymorphism (AFLP) to reconstruct the evolution of species within three genera of Lake Malawi sand-dwelling cichlids that construct elaborate male display platforms, or bowers. Sister taxa with distinct bower morphologies, and that exist in discrete leks separated by only 1-2 m of depth, are divergent in both sexually selected and ecological traits. Our phylogeny suggests that the forces of sexual and ecological selection are intertwined during the speciation of this group and that specific bower characteristics and trophic morphologies have evolved repeatedly. These results suggest that trophic morphology and bower form may be inappropriate characters for delineating taxonomic lineages. Specifically the morphological characters used to describe the genera Lethrinops and Tramitichromis do not define monophyletic clades. Using a combination of behavioural and genetic characters, we were able to identify several cryptic cichlid species on a single beach, which suggests that sand dweller species richness has been severely underestimated.     

Intraspecific cone opsin expression variation in the cichlids of Lake Malawi

The expression of cone opsin genes is a primary determinant of the characteristics of colour vision. Interspecific variation in opsin expression is common in African cichlids. It is correlated with foraging among cichlids from Lake Malawi, and with ambient light environment among cichlids from Lake Victoria. In this study, we tested whether gene expression varied within species such that it might be important in contributing to divergence. We hypothesized that light attenuation with depth would be correlated with predictable changes in gene expression in Lake Malawi, and that this variation would tune visual sensitivities to match the ambient light environment. We observed significant differences in cone opsin expression in three different comparisons among populations of the same species. Higher LWS expression was found in shallow versus deep Copadichromis eucinostomus. In Metriaclima zebra, individuals from Zimbawe Rock expressed significantly more SWS2B than those from Thumbi West Island, although these locales have similar ambient light environments. Finally, Tropheops gracilior from deeper water had significantly more variation in expression than their shallow counterparts. These results support that gene expression varies significantly between populations of the same species. Surprisingly, these results could not be explained by predicted visual performance as models predicted that differential expression patterns did not confer sensitivity advantages at different depths. This suggested that expression variation did not confer a local sensitivity advantage. Therefore, our findings were contrary to a primary requirement of the sensory bias hypothesis. As such, other explanations for intraspecific gene expression variation need to be tested.     

Differences in sounds made by courting males of three closely related Lake Malawi cichlid species

Courtship sounds made by three sympatric cichlid species, Pseudotropheus zebra , P. callainos and an undescribed species known as P . 'zebra gold' were recorded and compared to investigate the potential role of acoustic signals in mate choice. Sounds were emitted during 'quiver' and 'circle' components of the male courtship display and consisted of rapidly repeated pulse units. Some sound variables differed significantly among species with P. callainos generally being separated from the other two species. This species produced sounds with higher peak frequency (for a given length) and lower number of pulses than P . 'zebra gold' and higher pulse durations than P. zebra . In addition, standard length was inversely related to peak frequency in both P . 'zebra gold' and P. callainos (this relation was not tested in P. zebra due to the small sample size). These differences might indicate different regimes of intraspecific sexual selection among the three species.     

Local habitat complexity correlates with song complexity in a vocally elaborate honeyeater

Song complexity is an important behavioural trait in songbirds, subject to sexual selection. Elucidation of intraspecific variation in song complexity can provide insights into its evolution. In this study, we investigated song complexity variation in tūī (Prosthemadera novaeseelandiae), a vocally complex songbird endemic to New Zealand. At two separate nature reserves, we recorded male songs in two habitat types: forest remnants with high habitat complexity, and open habitats with lower habitat complexity. Analyses indicated strong evidence that song complexity was higher in forest habitats. Possible explanations for this divergence include: (i) competition between individuals results in higher quality, dominant males with more complex songs occupying forest habitats, and less competitive males occupying open habitat zones; (ii) forest habitats provide more abundant resources therefore higher tūī density, resulting in more complex songs; and (iii) a higher abundance of food in dense forest habitats may reduce nutritional stress during development resulting in full development of song nuclei. However, these hypotheses on the drivers of habitat effects on tūī song complexity remain to be tested.     

Mexican Jay social group size varies with habitat in northeastern Mexico

ABSTRACT.   We evaluated the hypothesis that social group size in Mexican Jays ( Aphelocoma ultramarina ) varies with habitat structure. We counted the social group size of Mexican Jays over a range of elevations and forest types in a single mountain range in northern Mexico (Sierra El Carmen, Coahuila). Group size increased significantly with elevation, in contrast to a population of Mexican Jays in Arizona that showed no such trend in another study. Among the vegetation variables measured, those relating to size of pines and oaks were especially important in explaining variation in group size. Because acorns and pine nuts are a major part of the diet of Mexican Jays, sites with larger oaks and pines may produce larger nut crops and support larger groups of jays. Elevation did not significantly explain variance in group size after taking vegetation into account. We compared group size and habitat variation across different parts of the geographic range of Mexican Jays. Our analysis indicates that variation of social group size in Mexican Jays is influenced by habitat quality at both local and geographic scales. Detailed studies on habitat structure and demographics of this population are needed to further clarify aspects of habitat quality important to these jays, and the mechanisms by which variation in social structure is maintained.