DOCSLIB.ORG

Genetic and Developmental Origins of a Unique Foraging Adaptation in a Lake Malawi Cichlid Genus

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Genetic and Developmental Origins of a Unique Foraging Adaptation in a Lake Malawi Cichlid Genus Genetic and developmental origins of a unique foraging adaptation in a Lake Malawi cichlid genus Moira R. Conitha, Yinan Hub,c, Andrew J. Conithd, Maura A. Maginnisd, Jacqueline F. Webbb, and R. Craig Albertsond,1 aGraduate Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, MA 01003; bDepartment of Biological Sciences, University of Rhode Island, Kingston, RI 02881; cBiology Department, Boston College, Chestnut Hill, MA 02467; and dDepartment of Biology, University of Massachusetts, Amherst, MA 01003 Edited by Hopi E. Hoekstra, HHMI and Harvard University, Cambridge, MA, and approved May 29, 2018 (received for review November 13, 2017) Phenotypic novelties are an important but poorly understood from model organisms, which are selected in part because of their category of morphological diversity. They can provide insights into conserved phenotypes (16, 17). Additionally, novel phenotypes of- the origins of phenotypic variation, but we know relatively little ten have ancient origins and/or occur in lineages that are not about their genetic origins. Cichlid fishes display remarkable diversity amenable to laboratory investigations. Here, we address the origin in craniofacial anatomy, including several novelties. One aspect of this of a novel phenotype by identifying the genetic mechanisms un- variation is a conspicuous, exaggerated snout that has evolved in derlying tissue-level changes of a unique craniofacial morphology in a single Malawi cichlid lineage and is associated with foraging a genus of cichlid from Lake Malawi, Africa. Cichlids are an iconic model system for the study of rapid and specialization and increased ecological success. We examined the – developmental and genetic origins for this phenotype and found that extensive craniofacial diversification (18 20). Within Lake Malawi, the snout is composed of two hypertrophied tissues: the intermax- the genus Labeotropheus exhibits extreme craniofacial anatomy that illary ligament (IML), which connects the right and left sides of the defines the boundary of cichlid morphospace (20). Among other extreme phenotypes, the two species in this genus possess an ex- upper jaw, and the overlying loose connective tissue. The IML is aggerated fleshy snout (e.g., Fig. 1A vs. Fig. 1B). We have previously present in all cichlids, but in its exaggerated form it interdigitates with shown that this elaborated snout folds in on itself, forming a flexible the more superficial connective tissue and anchors to the epithelium, flap that extends over the upper lip, sometimes reaching the distal forming a unique ligament–epithelial complex. We examined the β β → tip of the upper jaw dentition (21). It has been postulated that this EVOLUTION Transforming growth factor (Tgf ) Scleraxis (Scx) candidate path- protuberance enhances foraging efficiency by acting as a fulcrum to way and confirmed a role for these factors in snout development. We crop algae off rocks by leverage as an alternative to the energetically β demonstrate further that experimental up-regulation of Tgf is suffi- costly bite-and-twist mode of benthic feeding common in other cient to produce an expansion of scx expression and concomitant cichlid species (22). In addition, prior genetic work suggests that this changes in snout morphology. Genetic and genomic mapping show trait is under directional selection (21). Labeotropheus is also one of that core members of canonical Tgfβ signaling segregate with quan- the most ecologically successful genera in the lake, as it has a cos- titative trait loci (QTL) for snout variation. These data also implicate a mopolitan distribution and dominates the near shore rocky habitat candidate for ligament development, adam12, which we confirm us- (23). Indeed, although this trait is rare relative to the number of ing the zebrafish model. Collectively, these data provide insights into species that possess it (i.e., 2 of over 800 cichlid species in Lake ligament morphogenesis, as well as how an ecologically relevant Malawi), it is well represented in the lake given the ubiquity of novelty can arise at the molecular level. Labeotropheus. Thus, as with novelties in general, the evolution of this putatively adaptive structure is coincident with a unique for- evo-devo | craniofacial | ligament | TGFβ | novelty aging mode and expanded ecological success. pecies with novel phenotypes, which define the extremes of a Significance Scollective morphospace, are a valuable resource for research across disciplines. In evolutionary biology, this phenotypic class can Biologists have long been captivated by novel traits because they provide insights into the origins and constraints on morphological provide insights into both the origin of and constraints on mor- evolution (1–4). Engineers have long used novel phenotypes as in- phological variation. The iconic adaptive radiations of cichlid fishes spiration for biology-based design and technology (5, 6). Such have led to incredible diversity of form, including some species phenotypes can also serve as “evolutionary mutant models” of with an exaggerated snout. This novelty is mechanically in- disease states, whereby the adaptive trait mimics a maladaptive tegrated with the upper jaw, appears to be under directional se- condition in humans, and potentially provides insights into the ge- lection, and is found in one of the most ecologically successful netic factors relevant for disease prediction and management (7). cichlid lineages. We used protein manipulation, gene expression, Finally, bizarre phenotypes serve to captivate the public and engage and genetic mapping to implicate the Tgfβ pathway in the de- them in the context of education (8). velopment of this unusual trait. Given the functions of Tgfβ sig- Novel phenotypes can arise as a dramatic reconfiguration of naling in tissue proliferation, migration, invasion, and organ the body plan (e.g., seahorses), from the elaboration of existing fibrosis, this represents an example of the cooption of existing structures (e.g., ref. 9) or as de novo structures with no obvious pathways in the evolution of novelty. precursor (e.g., ref. 10). Likewise, regulation at the molecular level can occur as the recruitment of existing genes and signaling Author contributions: M.R.C. and R.C.A. designed research; M.R.C., Y.H., A.J.C., M.A.M., pathways (e.g., through changes in timing, location, or amount of J.F.W., and R.C.A. performed research; M.R.C., Y.H., A.J.C., J.F.W., and R.C.A. analyzed expression; refs. 9, 11, and 12) or by the evolution of new genes data; and M.R.C., A.J.C., and R.C.A. wrote the paper. (e.g., following gene/genome duplication events; refs. 13 and 14). The authors declare no conflict of interest. Unlike continuous phenotypic variation, novel morphologies This article is a PNAS Direct Submission. highlight the opportunistic and flexible nature of evolution to act This open access article is distributed under Creative Commons Attribution-NonCommercial- as both a tinkerer and an innovator (15). A major pursuit in NoDerivatives License 4.0 (CC BY-NC-ND). evolutionary developmental biology is to characterize the prox- 1To whom correspondence should be addressed. Email: [email protected]. imate genetic and developmental basis that can explain the ori- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. gin of novel phenotypes. However, our understanding remains 1073/pnas.1719798115/-/DCSupplemental. limited because most of our knowledge of development comes www.pnas.org/cgi/doi/10.1073/pnas.1719798115 PNAS Latest Articles | 1of6 Downloaded by guest on September 27, 2021 We hypothesized that this unique structure develops as an ex- pansion of the intermaxillary ligament, which runs laterally across the upper jaw and connects the left and right maxillary heads (24). Given the dynamic movement in fish skulls (25, 26), this class of tissue (e.g., ligaments) is likely to play important roles in foraging adaptations. However, relative to the bony skeleton, the evolution of ligaments is grossly understudied. Here, we employ a combination of genetic and developmental approaches to test the hypothesis that elaboration of the intermaxillary ligament in Labeotropheus occurs via expansion of the Tgfβ → Scx candidate pathway (27–31). Through these analyses, we also identified a previously unknown candidate for ligament hypertrophy, adam12, and verified its roles in ligament development via functional analyses using the zebrafish model. Together these data support our main hypothesis and contribute to an understanding of the genetic regulation of complex soft tissue morphologies and, more generally, of how phenotypic novelties evolve. Results and Discussion Anatomy and Development of the Snout. The snout in Labeotropheus is a complex and dynamic soft tissue structure compared with Tropheops, a closely related near ecological competitor that lacks an exaggerated snout (Fig. 1 A and B). Histological data showed two distinct, but interdigitating, tissue types within the snout—aDirect Red-positive organized connective tissue high in collagen (pink, Fig. 1 C and D) and an Alcian Blue-positive loose connective tissue (blue, Fig. 1 C and D). In both species, this basic configuration is maintained across the medio-lateral expanse of the snout, but for consistency we focused our comparisons between species and treatments on midline sections of this structure. The anatomy and organization of the Direct Red-positive tissue is consistent with ligamentous tissue.
Load more

Recommended publications
  • §4-71-6.5 LIST of CONDITIONALLY APPROVED ANIMALS November
    §4-71-6.5 LIST OF CONDITIONALLY APPROVED ANIMALS November 28, 2006 SCIENTIFIC NAME COMMON NAME INVERTEBRATES PHYLUM Annelida CLASS Oligochaeta ORDER Plesiopora FAMILY Tubificidae Tubifex (all species in genus) worm, tubifex PHYLUM Arthropoda CLASS Crustacea ORDER Anostraca FAMILY Artemiidae Artemia (all species in genus) shrimp, brine ORDER Cladocera FAMILY Daphnidae Daphnia (all species in genus) flea, water ORDER Decapoda FAMILY Atelecyclidae Erimacrus isenbeckii crab, horsehair FAMILY Cancridae Cancer antennarius crab, California rock Cancer anthonyi crab, yellowstone Cancer borealis crab, Jonah Cancer magister crab, dungeness Cancer productus crab, rock (red) FAMILY Geryonidae Geryon affinis crab, golden FAMILY Lithodidae Paralithodes camtschatica crab, Alaskan king FAMILY Majidae Chionocetes bairdi crab, snow Chionocetes opilio crab, snow 1 CONDITIONAL ANIMAL LIST §4-71-6.5 SCIENTIFIC NAME COMMON NAME Chionocetes tanneri crab, snow FAMILY Nephropidae Homarus (all species in genus) lobster, true FAMILY Palaemonidae Macrobrachium lar shrimp, freshwater Macrobrachium rosenbergi prawn, giant long-legged FAMILY Palinuridae Jasus (all species in genus) crayfish, saltwater; lobster Panulirus argus lobster, Atlantic spiny Panulirus longipes femoristriga crayfish, saltwater Panulirus pencillatus lobster, spiny FAMILY Portunidae Callinectes sapidus crab, blue Scylla serrata crab, Samoan; serrate, swimming FAMILY Raninidae Ranina ranina crab, spanner; red frog, Hawaiian CLASS Insecta ORDER Coleoptera FAMILY Tenebrionidae Tenebrio molitor mealworm,
    [Show full text]
  • Phylogeny of a Rapidly Evolving Clade: the Cichlid Fishes of Lake Malawi
    Proc. Natl. Acad. Sci. USA Vol. 96, pp. 5107–5110, April 1999 Evolution Phylogeny of a rapidly evolving clade: The cichlid fishes of Lake Malawi, East Africa (adaptive radiationysexual selectionyspeciationyamplified fragment length polymorphismylineage sorting) R. C. ALBERTSON,J.A.MARKERT,P.D.DANLEY, AND T. D. KOCHER† Department of Zoology and Program in Genetics, University of New Hampshire, Durham, NH 03824 Communicated by John C. Avise, University of Georgia, Athens, GA, March 12, 1999 (received for review December 17, 1998) ABSTRACT Lake Malawi contains a flock of >500 spe- sponsible for speciation, then we expect that sister taxa will cies of cichlid fish that have evolved from a common ancestor frequently differ in color pattern but not morphology. within the last million years. The rapid diversification of this Most attempts to determine the relationships among cichlid group has been attributed to morphological adaptation and to species have used morphological characters, which may be sexual selection, but the relative timing and importance of prone to convergence (8). Molecular sequences normally these mechanisms is not known. A phylogeny of the group provide the independent estimate of phylogeny needed to infer would help identify the role each mechanism has played in the evolutionary mechanisms. The Lake Malawi cichlids, however, evolution of the flock. Previous attempts to reconstruct the are speciating faster than alleles can become fixed within a relationships among these taxa using molecular methods have species (9, 10). The coalescence of mtDNA haplotypes found been frustrated by the persistence of ancestral polymorphisms within populations predates the origin of many species (11). In within species.
    [Show full text]
  • View/Download
    CICHLIFORMES: Cichlidae (part 5) · 1 The ETYFish Project © Christopher Scharpf and Kenneth J. Lazara COMMENTS: v. 10.0 - 11 May 2021 Order CICHLIFORMES (part 5 of 8) Family CICHLIDAE Cichlids (part 5 of 7) Subfamily Pseudocrenilabrinae African Cichlids (Palaeoplex through Yssichromis) Palaeoplex Schedel, Kupriyanov, Katongo & Schliewen 2020 palaeoplex, a key concept in geoecodynamics representing the total genomic variation of a given species in a given landscape, the analysis of which theoretically allows for the reconstruction of that species’ history; since the distribution of P. palimpsest is tied to an ancient landscape (upper Congo River drainage, Zambia), the name refers to its potential to elucidate the complex landscape evolution of that region via its palaeoplex Palaeoplex palimpsest Schedel, Kupriyanov, Katongo & Schliewen 2020 named for how its palaeoplex (see genus) is like a palimpsest (a parchment manuscript page, common in medieval times that has been overwritten after layers of old handwritten letters had been scraped off, in which the old letters are often still visible), revealing how changes in its landscape and/or ecological conditions affected gene flow and left genetic signatures by overwriting the genome several times, whereas remnants of more ancient genomic signatures still persist in the background; this has led to contrasting hypotheses regarding this cichlid’s phylogenetic position Pallidochromis Turner 1994 pallidus, pale, referring to pale coloration of all specimens observed at the time; chromis, a name
    [Show full text]
  • Biodiversity in Sub-Saharan Africa and Its Islands Conservation, Management and Sustainable Use
    Biodiversity in Sub-Saharan Africa and its Islands Conservation, Management and Sustainable Use Occasional Papers of the IUCN Species Survival Commission No. 6 IUCN - The World Conservation Union IUCN Species Survival Commission Role of the SSC The Species Survival Commission (SSC) is IUCN's primary source of the 4. To provide advice, information, and expertise to the Secretariat of the scientific and technical information required for the maintenance of biologi- Convention on International Trade in Endangered Species of Wild Fauna cal diversity through the conservation of endangered and vulnerable species and Flora (CITES) and other international agreements affecting conser- of fauna and flora, whilst recommending and promoting measures for their vation of species or biological diversity. conservation, and for the management of other species of conservation con- cern. Its objective is to mobilize action to prevent the extinction of species, 5. To carry out specific tasks on behalf of the Union, including: sub-species and discrete populations of fauna and flora, thereby not only maintaining biological diversity but improving the status of endangered and • coordination of a programme of activities for the conservation of bio- vulnerable species. logical diversity within the framework of the IUCN Conservation Programme. Objectives of the SSC • promotion of the maintenance of biological diversity by monitoring 1. To participate in the further development, promotion and implementation the status of species and populations of conservation concern. of the World Conservation Strategy; to advise on the development of IUCN's Conservation Programme; to support the implementation of the • development and review of conservation action plans and priorities Programme' and to assist in the development, screening, and monitoring for species and their populations.
    [Show full text]
  • Checklist of the Cichlid Fishes of Lake Malawi (Lake Nyasa)
    Checklist of the Cichlid Fishes of Lake Malawi (Lake Nyasa/Niassa) by M.K. Oliver, Ph.D. ––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––– Checklist of the Cichlid Fishes of Lake Malawi (Lake Nyasa/Niassa) by Michael K. Oliver, Ph.D. Peabody Museum of Natural History, Yale University Updated 24 June 2020 First posted June 1999 The cichlids of Lake Malawi constitute the largest vertebrate species flock and largest lacustrine fish fauna on earth. This list includes all cichlid species, and the few subspecies, that have been formally described and named. Many–several hundred–additional endemic cichlid species are known but still undescribed, and this fact must be considered in assessing the biodiversity of the lake. Recent estimates of the total size of the lake’s cichlid fauna, counting both described and known but undescribed species, range from 700–843 species (Turner et al., 2001; Snoeks, 2001; Konings, 2007) or even 1000 species (Konings 2016). Additional undescribed species are still frequently being discovered, particularly in previously unexplored isolated locations and in deep water. The entire Lake Malawi cichlid metaflock is composed of two, possibly separate, endemic assemblages, the “Hap” group and the Mbuna group. Neither has been convincingly shown to be monophyletic. Membership in one or the other, or nonendemic status, is indicated in the checklist below for each genus, as is the type species of each endemic genus. The classification and synonymies are primarily based on the Catalog of Fishes with a few deviations. All synonymized genera and species should now be listed under their senior synonym. Nearly all species are endemic to L. Malawi, in some cases extending also into the upper Shiré River including Lake Malombe and even into the middle Shiré.
    [Show full text]
  • Man Supplement
    Supplementary Materials for Whole Genome Sequences Of Malawi Cichlids Reveal Multiple Radiations Interconnected By Gene Flow Milan Malinsky, Hannes Svardal, Alexandra M. Tyers, Eric A. Miska, Martin J. Genner, George F. Turner, and Richard Durbin correspondence to: [email protected], [email protected] This PDF file includes: Materials and Methods Supplementary Text Figs. S1 to S32 Tables S1 to S8 Materials and Methods DNA extraction and sequencing: DNA was extracted from fin clips using the PureLink® Genomic DNA extraction kit (Life Technologies). Genomic libraries for paired-end sequencing on the Illumina HiSeq 2000 machine were prepared according to the Illumina TruSeq HT protocol to obtain paired-end reads with mean insert size of 300-500bp. As detailed in Supplementary Table 1, we used either Illumina HiSeq v3 chemistry (generating 100bp paired-end reads) or Illumina HiSeq v4 reagents (125bp paired-end reads). Low coverage (~6x) samples with v4 reagents were multiplexed 12 per lane. High coverage (~15x) v4 samples were multiplexed four per lane. For high coverage (~15x) v3 samples, a multiplexed library with 8 samples was sequenced over three lanes. The nine trio samples were multiplexed across eight lanes using the v3 chemistry, delivering approximately 40x coverage per individual. Raw data have been deposited at the NCBI Sequence Read Archive under BioProject PRJEB1254; sample accessions are listed in Table S4. Alignment: Reads were aligned to the Metriaclima zebra reference assembly version 1.111 (Table S5) using the bwa-mem v.0.7.10 algorithm82 with default options. For the trio parent samples that were used in the main analysis, we aligned data from only three of the eight lanes, aiming to have the same genome coverage for the trios as for the remaining (15x) samples.
    [Show full text]
  • Genetic and Developmental Origins of a Unique Foraging Adaptation in a Lake Malawi Cichlid Genus
    Genetic and developmental origins of a unique foraging adaptation in a Lake Malawi cichlid genus Moira R. Conitha, Yinan Hub,c, Andrew J. Conithd, Maura A. Maginnisd, Jacqueline F. Webbb, and R. Craig Albertsond,1 aGraduate Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, MA 01003; bDepartment of Biological Sciences, University of Rhode Island, Kingston, RI 02881; cBiology Department, Boston College, Chestnut Hill, MA 02467; and dDepartment of Biology, University of Massachusetts, Amherst, MA 01003 Edited by Hopi E. Hoekstra, HHMI and Harvard University, Cambridge, MA, and approved May 29, 2018 (received for review November 13, 2017) Phenotypic novelties are an important but poorly understood from model organisms, which are selected in part because of their category of morphological diversity. They can provide insights into conserved phenotypes (16, 17). Additionally, novel phenotypes of- the origins of phenotypic variation, but we know relatively little ten have ancient origins and/or occur in lineages that are not about their genetic origins. Cichlid fishes display remarkable diversity amenable to laboratory investigations. Here, we address the origin in craniofacial anatomy, including several novelties. One aspect of this of a novel phenotype by identifying the genetic mechanisms un- variation is a conspicuous, exaggerated snout that has evolved in derlying tissue-level changes of a unique craniofacial morphology in a single Malawi cichlid lineage and is associated with foraging a genus of cichlid from Lake Malawi, Africa. Cichlids are an iconic model system for the study of rapid and specialization and increased ecological success. We examined the – developmental and genetic origins for this phenotype and found that extensive craniofacial diversification (18 20).
    [Show full text]
  • Revised Diagnosis of Metriaclima with Description of a New Species (Teleostei: Cichlidae) from Lake Malawi National Park, Africa
    233 Ichthyol. Explor. Freshwaters, Vol. 17, No. 3, pp. 233-246, 11 fi gs., 2 tabs., September 2006 © 2006 by Verlag Dr. Friedrich Pfeil, München, Germany – ISSN 0936-9902 Revised diagnosis of Metriaclima with description of a new species (Teleostei: Cichlidae) from Lake Malawi National Park, Africa Adrianus F. Konings* and Jay R. Stauffer, Jr.** The diagnosis of Metriaclima is expanded to include several feeding behavioral characteristics. Species of Metria- clima feed at almost perpendicular angles to the substrate and are able to align the teeth of both upper and lower jaws in the same plane by abducting the jaws to a 180°-angle opening. While closing the mouth, the teeth comb through the algae anchored to the substrate and collect loose material. The bites to the substrate follow in rapid succession. We have further expanded the diagnosis of Metriaclima zebra to include a population without distinct vertical bars. Finally, we describe a new species, M. flavifemina, which inhabits the rock-sand interface in the southern part of the lake. Introduction a moderately-sloped ethmo-vomerine block with a swollen rostral tip. Morphological characteristics The small, rock-dwelling haplochromine cichlid of the feeding apparatus reflect the manner in fishes in Lake Malawi, Africa, are commonly which these fishes browse from the substrate and referred to as mbuna. The genus Pseudotropheus one of the purposes of this paper is to include – one of the dozen genera currently recognized characters of feeding behavior in the diagnosis of within the mbuna – originally included a widely Metriaclima. diverse group of cichlids and served as a catch-all When Stauffer et al.
    [Show full text]
  • Chromosome Differentiation Patterns During Cichlid Fish Evolution
    Poletto et al. BMC Genetics 2010, 11:50 http://www.biomedcentral.com/1471-2156/11/50 RESEARCH ARTICLE Open Access ChromosomeResearch article differentiation patterns during cichlid fish evolution Andréia B Poletto1, Irani A Ferreira1, Diogo C Cabral-de-Mello1, Rafael T Nakajima1, Juliana Mazzuchelli1, Heraldo B Ribeiro1, Paulo C Venere2, Mauro Nirchio3, Thomas D Kocher4 and Cesar Martins*1 Abstract Background: Cichlid fishes have been the subject of increasing scientific interest because of their rapid adaptive radiation which has led to an extensive ecological diversity and their enormous importance to tropical and subtropical aquaculture. To increase our understanding of chromosome evolution among cichlid species, karyotypes of one Asian, 22 African, and 30 South American cichlid species were investigated, and chromosomal data of the family was reviewed. Results: Although there is extensive variation in the karyotypes of cichlid fishes (from 2n = 32 to 2n = 60 chromosomes), the modal chromosome number for South American species was 2n = 48 and the modal number for the African ones was 2n = 44. The only Asian species analyzed, Etroplus maculatus, was observed to have 46 chromosomes. The presence of one or two macro B chromosomes was detected in two African species. The cytogenetic mapping of 18S ribosomal RNA (18S rRNA) gene revealed a variable number of clusters among species varying from two to six. Conclusions: The karyotype diversification of cichlids seems to have occurred through several chromosomal rearrangements involving fissions, fusions and inversions. It was possible to identify karyotype markers for the subfamilies Pseudocrenilabrinae (African) and Cichlinae (American). The karyotype analyses did not clarify the phylogenetic relationship among the Cichlinae tribes.
    [Show full text]
  • Whole-Genome Sequences of Malawi Cichlids Reveal Multiple Radiations Interconnected by Gene Flow
    ARTICLES https://doi.org/10.1038/s41559-018-0717-x Whole-genome sequences of Malawi cichlids reveal multiple radiations interconnected by gene flow Milan Malinsky 1,2,10*, Hannes Svardal 1,3,4,5,10, Alexandra M. Tyers6,9, Eric A. Miska 1,3,7, Martin J. Genner8, George F. Turner6 and Richard Durbin 1,3* The hundreds of cichlid fish species in Lake Malawi constitute the most extensive recent vertebrate adaptive radiation. Here we characterize its genomic diversity by sequencing 134 individuals covering 73 species across all major lineages. The aver- age sequence divergence between species pairs is only 0.1–0.25%. These divergence values overlap diversity within species, with 82% of heterozygosity shared between species. Phylogenetic analyses suggest that diversification initially proceeded by serial branching from a generalist Astatotilapia-like ancestor. However, no single species tree adequately represents all species relationships, with evidence for substantial gene flow at multiple times. Common signatures of selection on visual and oxygen transport genes shared by distantly related deep-water species point to both adaptive introgression and independent selec- tion. These findings enhance our understanding of genomic processes underlying rapid species diversification, and provide a platform for future genetic analysis of the Malawi radiation. he formation of every lake or island represents a fresh oppor- The species that comprise the radiation can be divided into seven tunity for colonization, proliferation and diversification of groups with differing ecology and morphology (see Supplementary Tliving forms. In some cases, the ecological opportunities pre- Note): (1) the rock-dwelling ‘mbuna’; (2) Rhamphochromis—typi- sented by underutilized habitats facilitate adaptive radiation—rapid cally midwater pelagic piscivores; (3) Diplotaxodon—typically deep- and extensive diversification of the descendants of the colonizing water pelagic zooplanktivores and piscivores; (4) deep-water and lineages1–3.
    [Show full text]
  • Attachment 1
    ZB13.6 TORONTO ZOO ANIMAL LIVES WITH PURPOSE INSTITUTIONAL ANIMAL PLAN 2020 OUR MISSION: Our Toronto Zoo - Connecting animals, people and conservation science to fight extinction OUR VISION: A world where wildlife and wild spaces thrive TABLE OF CONTENTS EXECUTIVE SUMMARY ....................................................................................................................... 3 Position Statement ............................................................................................................................. 4 A Living Plan ...................................................................................................................................... 4 Species Scoring and Selection Criteria .............................................................................................. 5 Themes and Storylines ....................................................................................................................... 7 African Rainforest Pavilion .................................................................................................................... 9 African Savanna .................................................................................................................................. 13 Indo-Malaya Pavilion ........................................................................................................................... 16 Eurasia Wilds ......................................................................................................................................
    [Show full text]
  • Constraint and Diversification of Developmental Trajectories in Cichlid Facial Morphologies Powder Et Al
    Constraint and diversification of developmental trajectories in cichlid facial morphologies Powder et al. Powder et al. EvoDevo (2015) 6:25 DOI 10.1186/s13227-015-0020-8 Powder et al. EvoDevo (2015) 6:25 DOI 10.1186/s13227-015-0020-8 RESEARCH Open Access Constraint and diversification of developmental trajectories in cichlid facial morphologies Kara E. Powder* , Kayla Milch, Garrett Asselin and R. Craig Albertson Abstract Background: A major goal of evolutionary biology is to understand the origins of phenotypic diversity. Changes in development, for instance heterochrony, can be a potent source of phenotypic variation. On the other hand, development can also constrain the spectrum of phenotypes that can be produced. In order to understand these dual roles of development in evolution, we examined the developmental trajectory of a trait central to the extensive adaptive radiation of East African cichlid fishes: craniofacial adaptations that allow optimal exploitation of ecological niches. Specifically, we use geometric morphometric analysis to compare morphological ontogenies among six species of Lake Malawi cichlids (n > 500 individuals) that span a major ecomorphological axis. We further evaluate how modulation of Wnt signaling impacts the long-term developmental trajectory of facial development. Results: We find that, despite drastic differences in adult craniofacial morphologies, there are general similarities in the path of craniofacial ontogeny among species, suggesting that natural selection is working within a conserved developmental program. However, we also detect species-specific differences in the timing, direction, and/or duration of particular developmental trajectories, including evidence of heterochrony. Previous work in cichlids and other systems suggests that species-specific differences in adult morphology are due to changes in molecular signaling pathways that regulate early craniofacial development.
    [Show full text]