The physiology of rapid ecological specialization: A look at the Midas cichlids

Understanding the process of speciation is a primary goal of evolutionary biology, yet the question of whether speciation can reach completion in the presence of gene flow remains controversial. For more than 50 years, the cichlids of Africa, and more recently those in South and Central America, have served as model systems for the study of speciation in nature. Cichlids are distinguished by their enormous species richness, their diversity of behavioural and trophic adaptations, and their rapid rate of divergence. In both Africa and South and Central America, the repeated interaction of geology, new founder events and adaptive evolution has created a series of natural experiments with speciation occurring both within and between waterbodies of differing ages. In the “From the Cover” paper in this issue of the Journal of Molecular Ecology, Raffini, Schneider, Franchini, Kautt and Meyer move beyond the question of which mechanisms drive speciation, and instead show that divergent morphologies and physiologies translate into adaptive traits. They investigate differences in physiology and gene expression profiles in a benthic/limnetic species pair of Midas cichlidsin a 24,000‐year‐old Nicaraguan crater lake. While recently diverged, these two species demonstrate significant ecological, but limited genetic differentiation. The authors find that the distinct morphotypes translate into relevant differences in swimming performance and metabolic rates that correspond to differential gene expression profiles. Hence, the authors take an integrative approach examining the impacts of morphological differences on performance and niche partitioning: an approach that can advance our understanding of the drivers of morphological and physiological divergence during speciation.     

Genome and cuticular hydrocarbon‐based species delimitation shed light on potential drivers of speciation in a Neotropical ant species complex

Geographic separation that leads to the evolution of reproductive isolation between populations generally is considered the most common form of speciation. However, speciation may also occur in the absence of geographic barriers due to phenotypic and genotypic factors such as chemical cue divergence, mating signal divergence, and mitonuclear conflict. Here, we performed an integrative study based on two genome‐wide techniques (3RAD and ultraconserved elements) coupled with cuticular hydrocarbon (CHC) and mitochondrial (mt) DNA sequence data, to assess the species limits within the Ectatomma ruidum species complex, a widespread and conspicuous group of Neotropical ants for which heteroplasmy (i.e., presence of multiple mtDNA variants in an individual) has been recently discovered in some populations from southeast Mexico. Our analyses indicate the existence of at least five distinct species in this complex: two widely distributed across the Neotropics, and three that are restricted to southeast Mexico and that apparently have high levels of heteroplasmy. We found that species boundaries in the complex did not coincide with geographic barriers. We therefore consider possible roles of alternative drivers that may have promoted the observed patterns of speciation, including mitonuclear incompatibility, CHC differentiation, and colony structure. Our study highlights the importance of simultaneously assessing different sources of evidence to disentangle the species limits of taxa with complicated evolutionary histories.     

Novel trophic niches drive variable progress towards ecological speciation within an adaptive radiation of pupfishes

Adaptive radiation is recognized by a rapid burst of phenotypic, ecological and species diversification. However, it is unknown whether different species within an adaptive radiation evolve reproductive isolation at different rates. We compared patterns of genetic differentiation between nascent species within an adaptive radiation of Cyprinodon pupfishes using genotyping by sequencing. Similar to classic adaptive radiations, this clade exhibits rapid morphological diversification rates and two species are novel trophic specialists, a scale‐eater and hard‐shelled prey specialist (durophage), yet the radiation is <10 000 years old. Both specialists and an abundant generalist species all coexist in the benthic zone of lakes on San Salvador Island, Bahamas. Based on 13 912 single‐nucleotide polymorphisms (SNPs), we found consistent differences in genetic differentiation between each specialist species and the generalist across seven lakes. The scale‐eater showed the greatest genetic differentiation and clustered by species across lakes, whereas durophage populations often clustered with sympatric generalist populations, consistent with parallel speciation across lakes. However, we found strong evidence of admixture between durophage populations in different lakes, supporting a single origin of this species and genome‐wide introgression with sympatric generalist populations. We conclude that the scale‐eater is further along the speciation‐with‐gene‐flow continuum than the durophage and suggest that different adaptive landscapes underlying these two niche environments drive variable progress towards speciation within the same habitat. Our previous measurements of fitness surfaces in these lakes support this conclusion: the scale‐eating fitness peak may be more distant than the durophage peak on the complex adaptive landscape driving adaptive radiation.     

Phylogenetic relationships of species of Crenicichla (Teleostei: Cichlidae) from southern South America based on the mitochondrial cytochrome b gene

Phylogenetic analysis using Bayesian inference, likelihood and parsimony methods was conducted on 60 complete mitochondrial cytochrome b sequences from 21 species of Crenicichla, including all species known from Uruguay (Crenicichla celidochilus, Crenicichla lepidota Crenicichla minuano, Crenicichla missioneira, Crenicichla punctata, Crenicichla scottii, Crenicichla vittata), Crenicichla compressiceps, Crenicichla empheres, Crenicichla geayi, Crenicichla iguassuensis, Crenicichla macrophthalma, Crenicichla menezesi, Crenicichla notophthalmus, Crenicichla regani, Crenicichla cf. regani, Crenicichla semifasciata, Crenicichla sveni, Crenicichla tendybaguassu, two unidentified species, and also two species of Teleocichla. Bayesian analysis resulted in a trichotomy with three major groups: (1) The C. missioneira species group (C. celidochilus, C. empheres, C. minuano, C. missioneira, C. tendybaguassu, and an undescribed species analyzed); (2) a group of southern species (C. iguassuensis, C. punctata, C. scottii, C. vittata); and (3) a rather heterogeneous group comprising the type species C. macrophthalma, members of the Crenicichla reticulata species group (C. geayi, C. semifasciata), members of the Crenicichla wallacii species group (C. compressiceps, C. notophthalmus, C. regani, C. cf. regani), members of the Crenicichla saxatilis species group (C. lepidota, C. menezesi, C. sveni, C. sp.), and two species of Teleocichla. Parsimony jackknifing resulted in a quadritomy with: (1) C. macrophthalma, (2) Teleocichla, (3) the saxatilis + wallacii group species, and (4) the rest, which include C. geayi and C. semifasciata as sister group to a dichotomy with the C. missioneira group and the remaining southern species. The sequence variation within the C. missioneira group is remarkably minor despite considerable morphological differences, supporting the conclusion that it forms an endemic species flock in the Uruguay River basin. Previously proposed species groups within the speciose genus Crenicichla (more than 90 species known) are partly corroborated. However, C. celidochilus was not previously associated with the C. missioneira species group, and C. vittata has not previously been associated with C. scottii, C. iguassuensis, or C. punctata. Crenicichla lepidota, C. sveni, C. menezesi and C. sp. represent the C. saxatilis group. Species of small size, representing the C. wallacii species group and Teleocichla are characterized by very long branches, and the position of Teleocichla differed considerably between the Bayesian and parsimony trees. This finding does not invalidate Teleocichla but rather suggests that the several monophyletic major clades within Crenicichla may need nominal recognition. A putative hybrid specimen with a morphology combining components from C. vittata and C. scottii, but with a cytochrome b sequence from C. scottii was found in a sample from the Rio Quaraí/Cuareim. Another putative hybrid specimen with a unique morphology but a cytochrome b sequence agreeing with C. scottii was found in a sample from Maldonado, but no other Crenicichla species than C. scottii is known from that locality.     

The speciation view: Disentangling multiple causes of adaptive and non-adaptive radiation in terms of speciation

Biological diversification often includes burst of lineage splitting. Such “radiation” has been known to act as evolutionary arenas with the potential to generate unique phylogenetic clusters and further novel groups. Although these radiations when accompanied by ecological diversification, so-called “adaptive radiation” have persisted as a central premise in evolutionary biology, the ecological and genetic mechanism of such rapid diversification has remained unclear. There are several critical definitions for the pattern of adaptive radiation, and those provide delimitation of adaptive and non-adaptive radiation. That being said, only a few studies have provided any clear demarcations in our understanding of the adaptive and non-adaptive causes of radiation from the mechanism of speciation. Here, we review the current consensus for the causes of adaptive radiation, especially along with the recent theoretical synthesis of “ecological speciation.” Further, we suggest the signature of adaptive and non-adaptive radiation in the earliest stages of diversification from the viewpoint of speciation. These criteria from the speciation view are useful to find the cases with the signatures of adaptive/non-adaptive radiation.     

The contribution of post-copulatory mechanisms to incipient ecological speciation in sticklebacks

Ecology can play a major role in species diversification. As individuals are adapting to contrasting habitats, reproductive barriers may evolve at multiple levels. While pre-mating barriers have been extensively studied, the evolution of post-mating reproductive isolation during early stages of ecological speciation remains poorly understood. In diverging three-spined stickleback ecotypes from two lakes and two rivers, we observed differences in sperm traits between lake and river males. Interestingly, these differences did not translate into ecotype-specific gamete precedence for sympatric males in competitive in vitro fertilization experiments, potentially owing to antagonistic compensatory effects. However, we observed indirect evidence for impeded development of inter-ecotype zygotes, possibly suggesting an early stage of genetic incompatibility between ecotypes. Our results show that pre-zygotic post-copulatory mechanisms play a minor role during this first stage of ecotype divergence, but suggest that genetic incompatibilities may arise at early stages of ecological speciation.     

Trophic differentiation in the phylogenetically young Cyprinodon species flock (Cyprinodontidae, Teleostei) from Laguna Chichancanab (Mexico)

Analysis of the gut contents of six syntopic Cyprinodon species from Laguna Chichancanab, Mexico, shows that the supposed basal form, C. beltrani , feeds on detritus and has the longest gut. All other species have significantly shorter guts. Whereas C. simus exclusively ingests detritus despite short gut length, all other species additionally rely on different benthic invertebrates. Each species has developed specific preferences: C. labiosus (amphipods), C. verecundus (bivalves), C. maya (ostracods and gastropods) and C. esconditus (ostracods and chironomid larvae). However, all of them ingest a minimum of c. 40% detritus. According to Schoener's index, pairwise niche overlap varies from c. 40% to over 95% in the species flock. Contrary to this, there is almost no overlap between the members of the flock and the only other native fish species, Gambusia sexradiata , which feeds nearly exclusively on terrestrial arthropods dropping on the water surface. Recently, the cichlid genus Oreochromis and the characid Astyanax fasciatus gained access to the lake. The cichlids show moderate to high niche overlap, whereas in A. fasciatus it is low. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 125–134.     

A new pelagic predatory pike cichlid (Teleostei: Cichlidae: Crenicichla) from the C. mandelburgeri species complex with parallel and reticulate evolution

The Crenicichla mandelburgeri species complex from the Middle Paraná shows parallel evolution of ecomorphs to the unrelated C. missioneira species complex from the Uruguay River. In this article, we describe a new species from the C. mandelburgeri species complex that has evolved a parallel morphology and ecology to an unrelated species from the C. missioneira species complex (C. celidochilus). The new species is a pelagic predator that feeds predominantly on fishes and together with C. celidochilus is the only known pelagic species in the large riverine genus Crenicichla. The new species is endemic solely to a small tributary (the Urugua-í) of the Middle Paraná River where it is sympatric and partly syntopic with two other closely related endemic species that, however, differ strongly in their ecomorphologies (one is a generalistic invertivore and the other a specialized molluscivore). Mitochondrial DNA phylogeny finds the new species nested within the widespread C. mandelburgeri. Reduced genome-representation ddRAD analyses, however, demonstrate that this new species is of a hybrid origin and shares ancestry with C. ypo, one of the two studied sympatric species.

     

Systematics and evolution of the Disa draconis complex (Orchidaceae)

The systematic status of Disa draconis (L.f.) Sw. is revised following extensive field studies of population variation in the Western Cape, South Africa. Principal component and cluster analyses revealed clear distinctions between populations from sandplain, semi-arid and montane environments. Diagnostic characters were found in each of the population clusters indicating the existence of a species complex, rather than a single taxon as in the current taxonomy. We propose, therefore, that the name D. draconis (L.f.) Sw. be restricted to the individuals of the sandplain populations from which the type was collected. We reinstate an earlier name, Disa harveiana Lindl., to describe the montane populations which possess several autapomorphic characters. We also show that the geographical variation in spur length and flowering time within this species can be partitioned into two geographically distinct subspecies: D. harveiana subsp. harveiana and D. harveiana subsp. longicalcarata Johnson & Linder. The populations from the semi-arid Karoo region were recognized as a distinct new species, Disa karooica Johnson & Linder, on the basis of their peculiar petal structure. A cladistic analysis indicated that the three species forming the D. draconis complex form a monophyletic and relatively specialized lineage within Disa sect. Coryphaea. The revised classification also has important conservation implications as D. draconis , previously considered a common species, is now restricted to a few highly threatened populations on the west coast near Cape Town.     

Ancient lakes revisited: from the ecology to the genetics of speciation

Explosive speciation in ancient lakes has fascinated biologists for centuries and has inspired classical work on the tempo and modes of speciation. Considerable attention has been directed towards the extrinsic forces of speciation—the geological, geographical and ecological peculiarities of ancient lakes. Recently, there has been a resurgence of interest in the intrinsic nature of these radiations, the biological characteristics conducive to speciation. While new species are thought to arise mainly by the gradual enhancement of reproductive isolation among geographically isolated populations, ancient lakes provide little evidence for a predominant role of geography in speciation. Recent phylogenetic work provides strong evidence that multiple colonization waves were followed by parallel intralacustrine radiations that proceeded at relatively rapid rates despite long‐term gene flow through hybridization and introgression. Several studies suggest that hybridization itself might act as a key evolutionary mechanism by triggering major genomic reorganization/revolution and enabling the colonization of new ecological niches in ancient lakes. These studies propose that hybridization is not only of little impediment to diversification but could act as an important force in facilitating habitat transitions, promoting postcolonization adaptations and accelerating diversification. Emerging ecological genomic approaches are beginning to shed light on the long‐standing evolutionary dilemma of speciation in the face of gene flow. We propose an integrative programme for future studies on speciation in ancient lakes.     

Adaptive loss of an old duplicated gene during incipient speciation

To probe the role of natural selection in species origin, we performed a DNA polymorphism survey of the Drosophila melanogaster desaturase2 (ds2) locus. ds2 is responsible for a cuticular hydrocarbon difference between two behaviorally isolated races--Zimbabwe (Z) and Cosmopolitan (M). The ds2 allele prevalent in the Z populations is functional, while the allele from the M populations harbors a 16-bp deletion upstream of the gene which knocks out its expression. We find a signature of positive selection in the ds2 promoter, but not in the control gene, sas. This signature appears to be confined to the derived M population. We also find that the selection has been recent because the gene retains a signature of a selective sweep evidenced by the departure of Fay and Wu's H test from neutral expectation. We also find that ds2, as well as its duplicate pair ds1, has been maintained in the Drosophila genus for at least 40 Myr without any sign of adaptive change. Taken together with previous molecular genetic evidence, our results suggest that ds2 is one of the genes responsible for adaptive divergence of the Z and M races of D. melanogaster.     

Along the speciation continuum in sticklebacks

Speciation can be viewed as a continuum, potentially divisible into several states: (1) continuous variation within panmictic populations, (2) partially discontinuous variation with minor reproductive isolation, (3) strongly discontinuous variation with strong but reversible reproductive isolation and (4) complete and irreversible reproductive isolation. Research on sticklebacks (Gasterosteidae) reveals factors that influence progress back and forth along this continuum, as well as transitions between the states. Most populations exist in state 1, even though some of these show evidence of disruptive selection and positive assortative mating. Transitions to state 2 seem to usually involve strong divergent selection coupled with at least a bit of geographic separation, such as parapatry (e.g. lake and stream pairs and mud and lava pairs) or allopatry (e.g. different lakes). Transitions to state 3 can occur when allopatric or parapatric populations that evolved under strong divergent selection come into secondary contact (most obviously the sympatric benthic and limnetic pairs), but might also occur between populations that remained in parapatry or allopatry. Transitions to state 4 might be decoupled from these selective processes, because the known situations of complete, or nearly complete, reproductive isolation (Japan Sea and Pacific Ocean pair and the recognized gasterosteid species) are always associated with chromosomal rearrangements and environment‐independent genetic incompatibilities. Research on sticklebacks has thus revealed complex and shifting interactions between selection, adaptation, mutation and geography during the course of speciation.     

Phylogenomic analysis suggests Coreidae and Alydidae (Hemiptera: Heteroptera) are not monophyletic

Next‐generation sequencing technologies (NGS) allow systematists to amass a wealth of genomic data from non‐model species for phylogenetic resolution at various temporal scales. However, phylogenetic inference for many lineages dominated by non‐model species has not yet benefited from NGS, which can complement Sanger sequencing studies. One such lineage, whose phylogenetic relationships remain uncertain, is the diverse, agriculturally important and charismatic Coreoidea (Hemiptera: Heteroptera). Given the lack of consensus on higher‐level relationships and the importance of a robust phylogeny for evolutionary hypothesis testing, we use a large data set comprised of hundreds of ultraconserved element (UCE) loci to infer the phylogeny of Coreoidea (excluding Stenocephalidae and Hyocephalidae), with emphasis on the families Coreidae and Alydidae. We generated three data sets by including alignments that contained loci sampled for at least 50%, 60%, or 70% of the total taxa, and inferred phylogeny using maximum likelihood and summary coalescent methods. Twenty‐six external morphological features used in relatively comprehensive phylogenetic analyses of coreoids were also re‐evaluated within our molecular phylogenetic framework. We recovered 439–970 loci per species (16%–36% of loci targeted) and combined this with previously generated UCE data for 12 taxa. All data sets, regardless of analytical approach, yielded topologically similar and strongly supported trees, with the exception of outgroup relationships and the position of Hydarinae. We recovered a monophyletic Coreoidea, with Rhopalidae highly supported as the sister group to Alydidae + Coreidae. Neither Alydidae nor Coreidae were monophyletic; the coreid subfamilies Hydarinae and Pseudophloeinae were recovered as more closely related to Alydidae than to other coreid subfamilies. Coreinae were paraphyletic with respect to Meropachyinae. Most morphological traits were homoplastic with several clades defined by few, if any, synapomorphies. Our results demonstrate the utility of phylogenomic approaches in generating robust hypotheses for taxa with long‐standing phylogenetic problems and highlight that novel insights may come from such approaches.     

Habitat use and its implications to functional morphology: niche partitioning and the evolution of locomotory morphology in Lake Tanganyikan cichlids (Perciformes: Cichlidae)

Animal locomotory morphology, i.e. morphological features involved in locomotion, is under the influence of a diverse set of ecological and behavioral factors. In teleost fish, habitat choice and foraging strategy are major determinants of locomotory morphology. In this study, we assess the influence of habitat use and foraging strategy on important locomotory traits, namely the size of the pectoral and caudal fins and the weight of the pectoral fin muscles, as applied to one of the most astonishing cases of adaptive radiation: the species flock of cichlid fishes in East African Lake Tanganyika. We also examine the course of niche partitioning along two main habitat axes, the benthic vs. limnetic and the sandy vs. rocky substrate axis. The results are then compared with available data on the cichlid adaptive radiation of neighbouring Lake Malawi. We find that pectoral fin size and muscle weight correlate with habitat use within the water column, as well as with substrate composition and foraging strategies. Niche partitioning along the benthic–limnetic axis in Lake Tanganyikan cichlids seems to follow a similar course as in Lake Malawi, while the course of habitat use with respect to substrate composition appears to differ between the cichlid assemblages of these two lakes.     

Sexual selection,reproductive behavior,and speciation in the mbuna species flock of Lake Malawi (Pisces: Cichlidae)

Synopsis The cichlid species flocks of the African Great Lakes represent the most extreme case of adaptive radiation among vertebrates. Recently, attention has focused on the potential for sexual selection to drive or accelerate speciation in these fishes. Cichlids as a whole are social in nature and display complex behavior, particularly during courtship and spawning; however, the extent to which changes in species recognition cues may account for species diversity among haplochromine lineages has remained speculative. Our investigations have indicated that oral incubating haplochromines show a reduction in diversity and extent of courtship relative to substrate brooding cichlids, and apparently retain aspects of a primitive specific mate recognition system. Laboratory observations of courtship in the Malawian endemicPseudotropheus zebra suggest that organization of the spawning bout is loose, and lacking in any well defined stimulus-response chain. Interspecific comparisons of in situ courtship behavior among male mbuna, lithophilous haplochromines of Lake Malawi, revealed only one potential example of species-specific behavior, and indicated that mate choice occurred prior to the onset of intense courtship. Courtship display by male mbuna does not appear critical to species recognition and may represent an evolutionary relict. Alternatively, male courtship display may have an indirect effect on successful reproduction or may be maintained through pleiotropic effects. The mbuna display no evidence of behavioral innovation and show limited interspecific differentiation in behavioral expression. More generally, there is no evidence at present to suggest that epigamic sexual selection, acting on courtship behavior, has been a major mechanism in the diversification of the haplochromine species flocks.     

The origin of two cryptic species of African desert jerboas (Dipodidae: Jaculus)

The desert biota is exposed to extreme and variable conditions that shape its evolution and diversification processes. In this respect, the Jaculus jerboas have gained the attention of researchers as a result of their broad Saharan–Arabian distribution and their high and unexplained, morphological, anatomical, and molecular variation. In the present study, mitochondrial and nuclear genealogies where used to confirm monophyly of two cryptic species: Jaculus jaculus and Jaculus deserti. The reconstructed demography showed that the evolutionary histories of the species are markedly different and that the expansion into North‐West Africa by J. deserti was more recent than that of J. jaculus. The weak ecological separation between species and the signs of recent population growth and expansion of J. deserti suggest that its sympatric occurrence with J. jaculus is recent and that these species evolved in isolated populations, after diverging around the Pliocene–Pleistocene boundary. The importance of climate changes on the Sahara Desert biota is discussed in the context of genetic diversification. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 435–445.     

The birth of an endemic species flock: demographic history of the Bellamya group (Gastropoda,Viviparidae) in Lake Malawi

Changes in habitat stability may significantly shape evolutionary patterns and processes in ancient lakes. In the present study, we use a hierarchical combination of molecular phylogenetic and coalescent approaches to investigate the evolutionary history of the endemic species of the gastropod genus Bellamya in the African rift‐lake Malawi. By integrating our findings with reported palaeontological and palaeolimnological data, we demonstrate that all but one evolutionary lineage of the Pliocene Bellamya fauna in Lake Malawi became extinct. Coalescent analyses indicate that the modern radiation underwent both a sudden demographic and a spatial expansion after a genetic bottleneck. We argue that a reflooding of the lake after severe Pleistocene low stands offers a straightforward explanation for this pattern and may have triggered speciation processes in the modern endemic Bellamya radiation in Lake Malawi. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 130–143.