Hernán López-Fernández

Habitat structural complexity and morphological diversity of fish assemblages in a Neotropical floodplain river

High species richness and evenness in structurally complex habitats has been hypothesized to be associated with niche partitioning. To test this idea, relationships between habitat structural complexity in river littoral-zone habitats and morphological diversity of tropical fishes were examined in the Cinaruco River, Venezuela. Six habitat attributes were quantified in 45 sites spanning a range of structural complexity. Fishes were collected during day and night to estimate species density and relative abundances at each site. Twenty-two morphological variables were measured for each species. Principal components analysis (PCA) of physical habitat data yielded two axes that modeled >80% of variation across sites. The first two axes from PCA of fish morphological variables modeled >70% of variation. Species density during both day and night was negatively associated with flow velocity and positively associated with habitat complexity. Similarity of day and night samples from the same site was significantly greater for sites with high habitat complexity and low flow. In general, mean local assemblage morphological PC scores were not significantly associated with habitat PC scores. Average, maximum, and standard deviation of morphological Euclidean distances of local assemblages revealed positive associations with structural complexity and negative associations with flow. These relationships held even when the positive relationship of species density was statistically removed from assemblage morphological patterns. Findings suggest that both species niche compression and assemblage niche space increase when habitat complexity is greater and flow velocity is lower in this tropical lowland river.

TESTING FOR ANCIENT ADAPTIVE RADIATIONS IN NEOTROPICAL CICHLID FISHES

Most contemporary studies of adaptive radiation focus on relatively recent and geographically restricted clades. It is less clear whether diversification of ancient clades spanning entire continents is consistent with adaptive radiation. We used novel fossil calibrations to generate a chronogram of Neotropical cichlid fishes and to test whether patterns of lineage and morphological diversification are congruent with hypothesized adaptive radiations in South and Central America. We found that diversification in the Neotropical cichlid clade and the highly diverse tribe Geophagini was consistent with diversity‐dependent, early bursts of divergence followed by decreased rates of lineage accumulation. South American Geophagini underwent early rapid differentiation in body shape, expanding into novel morphological space characterized by elongate‐bodied predators. Divergence in head shape attributes associated with trophic specialization evolved under strong adaptive constraints in all Neotropical cichlid clades. The South American Cichlasomatini followed patterns consistent with constant rates of morphological divergence. Although morphological diversification in South American Heroini was limited, Eocene invasion of Central American habitats was followed by convergent diversification mirroring variation observed in Geophagini. Diversification in Neotropical cichlids was influenced by the early adaptive radiation of Geophagini, which potentially limited differentiation in other cichlid clades.

Accelerated Mitochondrial Evolution and Darwin's Corollary : Asymmetric Viability of Reciprocal F1 Hybrids in Centrarchid Fishes

Reciprocal crosses between species can yield hybrids with different viabilities. The high frequency of this asymmetric hybrid viability (“Darwins corollary”) places it alongside Haldanes rule and the “large-X effect” as a general feature of postmating reproductive isolation. Recent theory suggests that reciprocal cross asymmetries can arise from stochastic substitutions in uniparentally inherited loci such as mitochondrial genomes, although large systematic differences in mitochondrial substitution rates can also contribute to asymmetries. Although the magnitude of asymmetry will be relatively insensitive to unequal rates of mitochondrial evolution in diverging species, we show here that rate asymmetries can have a large effect on the direction of viability asymmetries. In reciprocal crosses between species, the maternal parent with faster mitochondrial evolution will tend to produce less viable F1 hybrids owing to an increased probability of mito-nuclear incompatibilities. We test this prediction using data on reciprocal hybrid viability and molecular evolution rates from a clade of freshwater fishes, Centrarchidae. As predicted, species with accelerated mitochondrial evolution tend to be the worse maternal parent for F1 hybrids, providing the first comparative evidence for a systematic basis to Darwins corollary. This result is consistent with the hypothesis that mito-nuclear incompatibilities can play an important role in reproductive isolation. Such asymmetrical reproductive isolation may help explain the asymmetrical mitochondrial introgression observed between many hybridizing species. However, as with any comparative study, we cannot rule out the possibility that our results arise from a mutual correlation with a third variable such as body size.

Evolutionary Perspectives on Seed Consumption and Dispersal by Fishes

ABSTRACT Fishes probably were the first vertebrate seed dispersers, yet little research has examined this phenomenon. We review evidence of fruit and seed consumption by fishes, and analyze the evolution of frugivory and granivory using South American serrasalmids as a model. Frugivory and granivory are observed among diverse fish taxa worldwide, although most reports are from the Neotropics. Frugivory and granivory among serrasalmids apparently are derived from omnivory, with powerful jaws and specialized dentition appearing as major adaptations. No particular fruit traits seem to be associated with seed dispersal by fishes (ichthyochory). Recent experimental evidence of ichthyochory suggests that fishes can influence riparian vegetation dynamics. Because of deleterious human impacts on aquatic ecosystems worldwide, many critical interactions between plants and fishes have been disrupted before they could be studied. Exotic frugivorous fishes have recently become established on foreign continents, with unknown ecological consequences.

Morphology, molecules, and character congruence in the phylogeny of South American geophagine cichlids (Perciformes, Labroidei)

Phylogenetic relationships among the Neotropical cichlid subfamily Geophaginae were examined using 136 morphological characters and a molecular dataset consisting of six mitochondrial and nuclear genes. Topologies produced by morphological and combined data under parsimony were contrasted, congruence among different partitions was analysed, and potential effects of character incongruence and patterns of geophagine evolution on phylogenetic resolution are discussed. Interaction of morphological and molecular characters in combined analysis produced better resolved and supported topologies than when either was analysed separately. Combined analyses recovered a strongly supported Geophaginae that was closely related to Cichlasomatinae. Within Geophaginae, two sister clades included all geophagine genera. Acarichthyini (Acarichthys+Guianacara) was sister to the ‘B clade’, which contained the ‘Geophagus clade’ (‘Geophagus’steindachneri+Geophagus sensu stricto, and both sister to Gymnogeophagus) as sister to the ‘Mikrogeophagus clade’ (Mikrogeophagus+‘Geophagus’brasiliensis), and in turn, the Geophagus and Mikrogeophagus clades were sister to the crenicarine clade (Crenicara+Dicrossus) and Biotodoma. The second geophagine clade included the ‘Satanoperca clade’ (Satanoperca+Apistogramma and Taeniacara) as sister to the ‘Crenicichla clade’ (Crenicichla+Biotoecus). Several lineages were supported by unique morphological synapomorphies: the Geophaginae + Cichlasomatinae (5 synapomorphies), Geophaginae (1), Crenicichla clade (3), crenicarine clade (1), the sister relationship of Apistogramma and Taeniacara (4) and of Geophagus sensu stricto and‘Geophagus’steindachneri (1), and the cichlasomine tribe Heroini (1). Incorporation of Crenicichla in Geophaginae reconciles formerly contradictory hypotheses based on morphological and molecular data, and makes the subfamily the most diverse and ecologically versatile clade of cichlids outside the African great lakes. Results of this study support the hypothesis that morphological differentiation of geophagine lineages occurred rapidly as part of an adaptive radiation.

Diet-Morphology Correlations in the Radiation of South American Geophagine Cichlids (Perciformes: Cichlidae: Cichlinae)

Genera within the South American cichlid tribe Geophagini display specialized feeding and reproductive strategies, with some taxa specialized for both substrate-sifting and mouth brooding. Several lineages within the clade also possess an epibranchial lobe (EBL), a unique pharyngeal structure that has been proposed to have a function in feeding and/or mouth brooding. A recently published genus-level phylogeny of Neotropical cichlids was used as the evolutionary framework for investigating the evolution of morphological features presumably correlated with diet and mouth brooding in the tribe Geophagini. We tested for possible associations between the geophagine epibranchial lobe and benthic feeding and mouth brooding. We also addressed whether the EBL may be associated with unique patterns of diversification in certain geophagine clades. Tests of binary character correlations revealed the EBL was significantly associated with mouth brooding. We also tested for a relationship between diet and morphology. We analyzed stomach contents and morphometric variation among 21 species, with data for two additional species obtained from the literature. Principal Components Analysis revealed axes of morphological variation significantly correlated with piscivory and benthivory, and both morphology and diet were significantly associated with phylogeny. These results suggest that the EBL could be an adaptation for either feeding or mouth brooding. The EBL, however, was not associated with species richness or accelerated rates of phyletic diversification.

Divergent Positive Selection in Rhodopsin from Lake and Riverine Cichlid Fishes

Studies of cichlid evolution have highlighted the importance of visual pigment genes in the spectacular radiation of the African rift lake cichlids. Recent work, however, has also provided strong evidence for adaptive diversification of riverine cichlids in the Neotropics, which inhabit environments of markedly different spectral properties from the African rift lakes. These ecological and/or biogeographic differences may have imposed divergent selective pressures on the evolution of the cichlid visual system. To test these hypotheses, we investigated the molecular evolution of the dim-light visual pigment, rhodopsin. We sequenced rhodopsin from Neotropical and African riverine cichlids and combined these data with published sequences from African cichlids. We found significant evidence for positive selection using random sites codon models in all cichlid groups, with the highest levels in African lake cichlids. Tests using branch-site and clade models that partitioned the data along ecological (lake, river) and/or biogeographic (African, Neotropical) boundaries found significant evidence of divergent selective pressures among cichlid groups. However, statistical comparisons among these models suggest that ecological, rather than biogeographic, factors may be responsible for divergent selective pressures that have shaped the evolution of the visual system in cichlids. We found that branch-site models did not perform as well as clade models for our data set, in which there was evidence for positive selection in the background. One of our most intriguing results is that the amino acid sites found to be under positive selection in Neotropical and African lake cichlids were largely nonoverlapping, despite falling into the same three functional categories: spectral tuning, retinal uptake/release, and rhodopsin dimerization. Taken together, these results would imply divergent selection across cichlid clades, but targeting similar functions. This study highlights the importance of molecular investigations of ecologically important groups and the flexibility of clade models in explicitly testing ecological hypotheses.

Ecological variation in South American geophagine cichlids arose during an early burst of adaptive morphological and functional evolution

Diversity and disparity are unequally distributed both phylogenetically and geographically. This uneven distribution may be owing to differences in diversification rates between clades resulting from processes such as adaptive radiation. We examined the rate and distribution of evolution in feeding biomechanics in the extremely diverse and continentally distributed South American geophagine cichlids. Evolutionary patterns in multivariate functional morphospace were examined using a phylomorphospace approach, disparity-through-time analyses and by comparing Brownian motion (BM) and adaptive peak evolutionary models using maximum likelihood. The most species-rich and functionally disparate clade (CAS) expanded more efficiently in morphospace and evolved more rapidly compared with both BM expectations and its sister clade (GGD). Members of the CAS clade also exhibited an early burst in functional evolution that corresponds to the development of modern ecological roles and may have been related to the colonization of a novel adaptive peak characterized by fast oral jaw mechanics. Furthermore, reduced ecological opportunity following this early burst may have restricted functional evolution in the GGD clade, which is less species-rich and more ecologically specialized. Patterns of evolution in ecologically important functional traits are consistent with a pattern of adaptive radiation within the most diverse clade of Geophagini.

What Causes Partial F1 Hybrid Viability? Incomplete Penetrance versus Genetic Variation

Background Interspecific hybrid crosses often produce offspring with reduced but non-zero survivorship. In this paper we ask why such partial inviability occurs. This partial inviability could arise from incomplete penetrance of lethal Dobzhansky-Muller incompatibilities (DMIs) shared by all members of a hybrid cross. Alternatively, siblings may differ with respect to the presence or number of DMIs, leading to genotype-dependent variation in viability and hence non-Mendelian segregation of parental alleles in surviving F1 hybrids. Methodology/Principal Findings We used amplified fragment length polymorphisms (AFLPs) to test for segregation distortion in one hybrid cross between green and longear sunfish (Lepomis cyanellus and L. megalotis). Hybrids showed partial viability, and twice as much segregation distortion (36.8%) of AFLPs as an intraspecific control cross (18.8%). Incomplete penetrance of DMIs, which should cause genotype-independent mortality, is insufficient to explain the observed segregation distortion. Conclusions/Significance We conclude that F1 hybrid sunfish are polymorphic for DMIs, either due to sex-linked DMI loci (causing Haldanes Rule), or polymorphic autosomal DMI loci. Because few AFLP markers were sex-linked (2%), the most parsimonious conclusion is that parents may have been heterozygous for loci causing hybrid inviability.

A targeted next‐generation sequencing toolkit for exon‐based cichlid phylogenomics

Cichlid fishes (family Cichlidae) are models for evolutionary and ecological research. Massively parallel sequencing approaches have been successfully applied to study relatively recent diversification in groups of African and Neotropical cichlids, but such technologies have yet to be used for addressing larger‐scale phylogenetic questions of cichlid evolution. Here, we describe a process for identifying putative single‐copy exons from five African cichlid genomes and sequence the targeted exons for a range of divergent (>tens of millions of years) taxa with probes designed from a single reference species (Oreochromis niloticus, Nile tilapia). Targeted sequencing of 923 exons across 10 cichlid species that represent the familys major lineages and geographic distribution resulted in a complete taxon matrix of 564 exons (649 549 bp), representing 559 genes. Maximum likelihood and Bayesian analyses in both species tree and concatenation frameworks yielded the same fully resolved and highly supported topology, which matched the expected backbone phylogeny of the major cichlid lineages. This work adds to the body of evidence that it is possible to use a relatively divergent reference genome for exon target design and successful capture across a broad phylogenetic range of species. Furthermore, our results show that the use of a third‐party laboratory coupled with accessible bioinformatics tools makes such phylogenomics projects feasible for research groups that lack direct access to genomic facilities. We expect that these resources will be used in further cichlid evolution studies and hope the protocols and identified targets will also be useful for phylogenetic studies of a wider range of organisms.