Phyloepigenetics IV: Lagartija y nemátodo

Herrel et al 2008. Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. Proc Natl Acad Sci U S A. Mar 25;105(12):4792-5.

Excerpts!

"In 1971 five adult pairs of this species were moved from the small islet of Pod Kopiste (0.09 km2) to the nearby Pod Mrcaru (0.03 km2) by Nevo and coworkers (...). Although the islet of Pod Mrcaru was originally inhabited by another lacertid lizard species (Podarcis melisellensis), repeated visits (twice yearly over the past three years, beginning in 2004) show that this species has become extinct on Pod Mrcaru. Genetic mitochondrial DNA analyses indicate that the lizards currently on Pod Mrcaru are indeed P. sicula and are genetically indistinguishable from lizards from the source population"


"Differences in head size and shape also translate into significant dif ferences in bite force bet ween populations. Our data show that P. sicula lizards consume more plant material on Pod Mrcaru compared with the ancestral population on Pod Kopiste"


"This shift to a predominantly plant-based diet has resulted in the dramatic evolution of intestinal morpholog y. Morphological analysis of preserved specimens shows the presence of cecal valves (Fig. 4) in all individuals, including a hatchling (26.4-mm snout-vent length, umbilical scar present) and a very young juvenile (33.11-mm snout-vent length) examined from Pod Mrcaru."


"The fact that 1% of all currently known species of squamates have cecal valves (13, 14) illustrates the unusual nature of these structures in this population"

"Cecal valves slow down food passage and provide for fermenting chambers, allowing commensal microorganisms to convert cellulose to volatile fatt y acids (15, 16). Indeed, in the lizards f rom Pod Mrcaru, nematodes were common in the hindgut but absent from individuals f rom PodKopiste"

"Because of the larger food base available and the increase in the predict abilit y of the food source, lizard densities on Pod Mrcaru are much greater (..) lizards on Pod Mrcaru do no longer appear to defend territories. Moreover, changes in foraging style (browsing versus active pursuit of mobile prey) and social structure may also have resulted in the dramatic changes in limb proportions and maximal sprint speed previously documented for this population"

"Although the presence of cecal valves and large heads in hatchlings and juveniles suggests a genetic basis for these differences, further studies investigating the potential role of phenotypic plasticity and/or maternal effects in the divergence bet ween populations are needed"

Herrell no discute mucho qué tan relevante puede ser la simbiosis con un nemátodo. Veamos un ejemplo de anfibios


Effects of the nematode Gyrinicola batrachiensis on development, gut morphology, and fermentation in bullfrog tadpoles (Rana catesbeiana): a novel mutualism


Gregory S. Pryor *, Karen A. Bjorndal J. Exp. Zool. 303A:704-712, 2005.


Abstract

We describe a novel mutualism between bullfrog tadpoles (Rana catesbeiana) and a tadpole-specific gastrointestinal nematode (Gyrinicola batrachiensis). Groups of tadpoles were inoculated with viable or nonviable nematode eggs, and development, morphology, and gut fermentation activity were compared between nematode-infected and uninfected tadpoles. Nematode infection accelerated tadpole development; the mean time to metamorphosis was 16 d shorter and the range of times to metamorphosis was narrower in nematode-infected tadpoles than in uninfected tadpoles. At metamorphosis, infected and uninfected bullfrogs did not differ in body size or condition. Colon width, wet mass of colon contents, and concentrations of most fermentation byproducts (short-chain fatty acids: SCFAs) in the hindgut were greater in infected tadpoles. Furthermore, in vitro fermentation yields for all SCFAs combined were over twice as high in infected tadpoles than in uninfected tadpoles. One explanation for accelerated development in infected tadpoles is the altered hindgut fermentation associated with the nematodes. Energetic contributions of fermentation were estimated to be 20% and 9% of the total daily energy requirement for infected and uninfected tadpoles, respectively. Infection by G. batrachiensis nematodes potentially confers major ecological and evolutionary advantages to R. catesbeiana tadpoles. The mutualism between these species broadens our understanding of the taxonomic diversity and physiological contributions of fermentative gut symbionts and suggests that nematodes inhabiting the gut regions of other ectothermic herbivores might have beneficial effects in those hosts.


Si bien algunos nemátodos son parásitos en reptiles, otros no lo son:


Oecologia. 2006 Dec;150(3):355-61. Epub 2006

O'Grady SP, Dearing MD. Isotopic insight into host-endosymbiont relationships in Liolaemid lizards

Nitrogen isotopes have been widely used to investigate trophic levels in ecological systems. Isotopic enrichment of 2-5 per thousand occurs with trophic level increases in food webs. Host-parasite relationships deviate from traditional food webs in that parasites are minimally enriched relative to their hosts. Although this host-parasite enrichment pattern has been shown in multiple systems, few studies have used isotopic relationships to examine other potential symbioses. We examined the relationship between two gut-nematodes and their lizard hosts. One species, Physaloptera retusa, is a documented parasite in the stomach, whereas the relationship of the other species, Parapharyngodon riojensis (pinworms), to the host is putatively commensalistic or mutualistic. Based on the established trophic enrichments, we predicted that, relative to host tissue, parasitic nematodes would be minimally enriched (0-1 per thousand), whereas pinworms, either as commensals or mutualists, would be significantly enriched by 2-5 per thousand. We measured the (15)N values of food, digesta, gut tissue, and nematodes of eight lizard species in the family Liolaemidae. Parasitic worms were enriched 1+/-0.2 per thousand relative to host tissue, while the average enrichment value for pinworms relative to gut tissue was 6.7+/-0.2 per thousand. The results support previous findings that isotopic fractionation in a host-parasite system is lower than traditional food webs. Additionally, the larger enrichment of pinworms relative to known parasites suggests that they are not parasitic and may be several trophic levels beyond the host.



Correlating diet and digestive tract specialization: Examples from the lizard family Liolaemidae

Shannon P. O’Gradya, Mariana Morandob, Luciano Avilab and M. Denise Dearinga
Zoology 2005, 108 : 201-210

Abstract

A range of digestive tract specializations were compared among dietary categories in the family Liolaemidae to test the hypothesis that herbivores require greater gut complexity to process plant matter. Additionally, the hypothesis that herbivory favors the evolution of larger body size was tested. Lastly, the association between diet and hindgut nematodes was explored. Herbivorous liolaemids were larger relative to omnivorous and insectivorous congeners and consequently had larger guts. In addition, small intestine length of herbivorous liolaemids was disproportionately longer than that of congeners. Significant interaction effects between diet and body size among organ dimensions indicate that increases in organ size occur to a greater extent in herbivores than other diet categories. For species with plant matter in their guts, there was a significant positive correlation between the percentage of plant matter consumed and small intestine length. Herbivorous liolaemids examined in this study lacked the gross morphological specializations (cecum and colonic valves) found in herbivores in the families Iguanidae and Agamidae. A significantly greater percentage of herbivorous species had nematodes in their gut. Of the species with nematodes, over 95% of herbivores had nematodes only in the hindgut. Prevalence of nematodes in the hindgut of herbivores was 2× that of omnivores and 4× that of insectivores.


Los dichosos nemátodos se encuentran en todas las especies de reptil que tienen válvulas cecales


Preguntas:


Todo este cambio, en sólo 34 años.... es acaso una acumulación por selección direccional de varios genes? Grano fino, o grano grueso?

Cuánto de este cambios fenotípico drástico se debe más bien al efecto inmediato de diferentes condiciones epigenéticas, como la mentada asociación con el nemátodo?

Origen simbiótico de un tipo celular: Los cnidocystos de cnidarios

Shostak S. 1993. A symbiogenetic theory for the origins of cnidocysts in Cnidaria. Biosystems 29(1):49-58

Abstract

Did cnidarian cnidocysts originate from cnidocyst-bearing protoctistans living as symbiotic partners with an epithelial placula? If an increase in the fitness of symbiotic partners was "locked in" by an evolutionary stable strategy, co-evolution and compartmentalization could have led phyletically separate, eukaryotic symbionts to fuse and undergo nuclear merger. Traits originating in the symbiotic partners would have been brought to the "synthetic" organism and reworked through evolution into the development of an integrated organism. Support for the theory of symbiogenetic origins of Cnidaria rests on traces of symbiosis detected in the relationship of cnidarian epithelium to interstitial cells (I-cells), the precursors of cnidocyst-producing cnidoblasts: (1) epithelium and I-cell are autonomous and differ in morphology, cellular dynamics, the relationship of differentiation to proliferation and the variety of cell types formed; (2) hydras and planulas can be "cured" of I-cells and their derivatives, thereby creating "epithelial" animals which lack responsiveness but retain vegetative properties. (3) The reintroduction of I-cells into "epithelial" animals which lack responsiveness but retain vegetative properties. (3) The reintroduction of I-cells into "epithelial" animals restores missing differentiated cell and organismic characteristics. Symbiogenesis as a source of metazoan species has consequences for concepts of development, from the origins of cell lines to the evolution of differentiation.

Aún no lo leo pero desde ya recuerdo el caso de que hay babosas de mar (moluscos nudibranquios) que habiéndose comido un cnidario antozoo recuperaban los cnidocystos creciéndolos en "cnidosacos" en el dorso...este hecho tan sorprendente puede hacer más sentido si consideramos que los cnidocystos de alguna forma son un linaje distinto que puede vivir tanto en el molusco como el cnidario. Digo nomás! Véase además este link

Post-Scriptum: He comenzado a leer apenas la introducción y ya me convencí. El abstract no menciona el "detalle" de la evidencia morfológica. Es contundente. Resulta que el cnidocisto ya existe en varios protoctistas por ej. dinoflagelados depredadores y myxosporidios donde se les conoce como tricocysto o cápsula polar (ver imagen a la derecha). Las semejazas entre cnidocistos, especialmente en proceso de desarrollo, son muchas a nivel de microsocpia electrónica, mecanismo de eyección (la presión hidrostática en la cápsula polar expulsa el filamento). En protoctistas myxosporideos o microsporideos puede haber división celular incompleta , compartiendo 2 o más nucleos o cápsulas polares; los cnidocystos forman "nidos" de células interconectadas (esta falta de respeto por los límites celulares también nos sugiere un posible mecanismo conducente a la eventual fusión al genoma del cnidario). Otro dato: hay dos grupos fundamentales de cnidoscystos en cnidarios, sólo un grupo en antozoarios, y ambos en medusas, que sugieren que pueden tratrase de simbiosis con dos distintos linajes de protoctistas.

Cnidocysto de Hydra formando su tubo externo. Engel et al. The EMBO Journal (2001) 20, 3063–3073

Horrid Phenotypic integration!

Since past centuries naturalist, Cirripedes (or barnacles) have been studied because their peculiar morphology and life cycle. They live in a calcareous shell like a mollusk as adults, and they have articulated biramous appendages like crustaceans. Thanks to the study of its development, through nauplius larva, it was possible to classify them as crustaceans. Whereas, they have an incomplete abdomen, lacking terminal segments present in other crustaceans.

Fig 1: Cirripedes drawn by Haeckel in his beautiful bool Kunstformen der Natur 1904. A parasitized crab by Sacculina sp. can bee seen in the center of the picture.

One of the strangest groups of cirripedes are the Rhizocephalan barnacles which are sessile adult parasites of other crustaceans with free-swimming larvae (Fig 1 and 2). Their mature females (called externa) are situated in the abdominal brood chamber of the host, lack even the rudiments of an alimentary canal and have neither excretory nor respiratory organs. But it penetrates it's hosts with a nutrient-absorbing system of rootlets, which possibley links the parasite to these functions in the host (Fig 2 ).

Fig 2: Peltogaster (Peltogastridae) whole externa and root system attached to a part of the main abdominal root trunk From Bresciani & Hoeg 2001.

The life cycle (Fig 3) of the parasite involves a mature female externa which is fertilized by one or two cryptic dwarf males and which subsequently releases a series of broods of free swimming nauplii. The nauplii develop lecithotrophically, metamorphose into cypris larvae after about 5–6 days and become competent to settle after another 3–4 days in the plankton. Female cypris larvae must locate a suitable host while the male cypris larvae must find a parasitized host containing a virgin female. Some of the sensory structures involved in this behavior are the lattice organs and the aesthetasc setae found on antennules of the cyprids that have been proposed as olfactory organs. Females possess one and the males two. It had been demonstrated that larvae can use waterborne host metabolites to find a suitable host.

Fig 3: Generic life cycle of Cirripedian parasite, from Øksnebjerg 1999.

Female cyprids settle on the exoskeleton of a host crab at the base of a plumose seta and metamorphose into a special stage known as the kentrogon. The kentrogon penetrates the exoskeleton of the crab with a hollow stylet and injects the primordial parasite into the hemocoelic fluid. After an internal phase of a few months to 3 years, the parasite produces an external virginal reproductive body (externa) situated under the abdomen of the host. The externa attracts male cyprids, which implant as dwarf males and remain with the female externa for the duration of the latter’s lifetime and fertilize all its broods. Externa failing to receive at least one male cannot mature and eventually perish, leaving a scar on the host exoskeleton.

Fig 4: First photo shows the cyprid larva, antennae are marked with arrows, from Pasternak et al 2005. Second photo shows the kentrogon stage injecting cells in to the host body, from Hoeg 1987.

Sacculina carcini is a rhizocephalan parasite that attacks the crab C. maenas. S. carcini can have on their hosts severe and lasting effects on these include growth, morphology, physiology, and behavior of the host crab. The parasite can arrest the moult cycle of its host crab (which therefore suffers increased fouling). As a consequence of rootlet growth this parasite castrates both male and female hosts and phenotypically feminizes the males. Both sexes suffer alterations in behavior such as response to the externa and Sacculina eggs as their own brood. For example a common behavior of fecunded female crabs is to climb to some high rock and groom its abdomen to release the fertilized eggs from the brood pouch. Moving her claw the mother crab stir the water generating a flow. In the same way male parasitized by Sacculina will display a similiar behavior when the parasite offpring is ready to hatch, he will groom the Externa and release the next generation of his foster sons. “Sacculinized” host became an integrated developmental system that include the castrated crab, the breeding externa and the dwarf males. These creatures had been the focus of interesting cromosome and molecular studies that we can discuss in a next episode.

Fig 5: Rhizocephalan Extena on infected host species showing rootlets distribution in different parasite-host systems: A: Peltogaster paguri (Peltogastridae) on Pagurus bernhardus. B: Sacculina carcini (Sacculinidae) on Carcinus maenas. C: Sylon hippolytes (Clistosaccidae) on Spirontocaris lilljeborgi, from Bresciani & Hoeg 2001.

Cristian Villagra

References:

Bresciani J & Høeg JT (2001) Comparative Ultrastructure of the Root System in Rhizocephalan Barnacles (Crustacea: Cirripedia: Rhizocephala). Journal of Morphology, 249:9–42.

Herberts C (1982) Host-Parasite Relation between the Shore Crab Carcinus maenas and Sacculina carcini (Rhizocephala): Identification and Characterization of a Specific Fraction Correlated with Parasitism. Journal of Invertebrate Pathology, 39, 60-65.

Hoeg JT (1987) The relation between cypris ultrastructure and metamorphosis in male and female Sacculina carcini (Crustacea, Cirripedia). Zoomorphology, 107:299-311.

Le Mouchel-Vielh E, Rigolot C, Gibert J-M & Deutsch JS (1998) Molecules and the Body Plan: The Hox Genesof Cirripedes (Crustacea). Molecular Phylogenetics and Evolution, 9,382–389.

Øksnebjerg B (1999) The Rhizocephala (Crustacea: Cirripedia) of the Mediterranean and black seas: taxonomy, biogeography and ecology. Israel Journal of Zoology, 46: 1-102.

Pasternak Z, Garm A & Høeg JT (2005) The morphology of the chemosensory aesthetasc-like setae used during settlement of cypris larvae in the parasitic barnacle Sacculina carcini (Cirripedia: Rhizocephala). Marine Biology, 146: 1005–1013.

Threshera RE, Wernerb M, Høegc JT, Svaned I, Glennerc H, Murphy NE, Wittwer C (2000) Developing the options for managing marine pests: specificity trials on the parasitic castrator, Sacculina carcini, against the European crab, Carcinus maenas, and relatedspecies. Journal of Experimental Marine Biology and Ecology, 254: 37–51

Strathmann RR (1993) Hypotheses on the Origins of Marine Larvae. Annual Review of Ecology and Systematics, 24: 89-117. Walker G(1985) The cypris larvaea of sacculina carcini Thompson (Crustacea: Cirripedia: Rhizocephala) J. Eq. Mar. hoI. Ecof, 93:131-145.

Cão Parasita (Perro Parásito)

Setembro passado, um artigo de capa da Cell chamou a atenção e ganhou as manchetes dos jornais: um estudo sobre um tumor sexualmente transmissível em cães (canine transmissible venereal tumour- CTVT). O CTVT havia sido caracterizado há 130 anos. Ele foi interpretado como um tumor capaz de transplantar-se para outro indivíduo. Uma metástase inter-individual, digamos (surpreendentemente, os CTVT não enfrentam todos os problemas imunológicos que acontecem quando realizamos transplantes de órgãos e tecidos).

Murin e colaboradores (2006) mostram que os CTVT representam uma linhagem celular antiga, distinta (aneuploide) e estável. Comparando o genoma dos CTVTs encontrados em cães de diferentes locais do mundo, perceberam que o genoma dos CTVTs são praticamente idênticos e muito distintos do genoma de seus hospedeiros. Os CTVTs seriam um conjunto de células somáticas que se segregam independentemente há no máximo 2500 anos.

Na última edição da revista Evolution & Development, Uri Frank oferece uma interpretação radical e curiosa. Inicialmente, Frank trata de descaracterizar o CTVT como um tumor. Em seguida vem o surpreendente: ele o caracteriza como uma nova espécie.

"This may lead us to the inevitable conclusion that CTVT is a new species (to be named) of parasitic dog that evolved very recently (and indeed very fast) to become established worldwide. It has undergone major changes in its developmental plan resulting in a completely different morphology and life cycle as compared with its free-living ancestor"

Como Frank chama atenção, grandes simplificações morfológicas ocorreram em outras linhagem (Ele cita Buddenbrockia. Eu incluiria Placozoa, Myxozoa, Micrognathozoa e outras esquisitices). Em uma análise filogenética, o CTVTs individuais formariam um clado monofilético com os cães domésticos, deixando os lobos como grupo irmão. Casos semelhantes são reportados no syrian hamsters e no diabo da tasmânia.


P.S. Nova espécie ou não, alguém sente falta da seleção natural para explicar este fenômeno?

Murgia, C., Pritchard, J. K., Kim, S. Y., Fassati, A., and Weiss, R. A. 2006. Clonal origin and evolution of a transmissible cancer. Cell 126: 477–487
Frank, U. The evolution of a malignant dog. Evolution & Development, v.9, n.6, p.521-522. 2007.

Misterios de las lampreas

Lamprea de río


Lamprea de mar

Las lampreas son archiconocidas por su pintoresco estilo de vida semiparasitario; lo que es menos sabido es que las lampreas parasitarias corresponden sólo a las lampreas marinas (que más bien son anádromas, es decir, inician su vida en el río y luego viven en el mar). Existen además lampreas que viven exclusivamente en los ríos y que jamás atacan a nadie. Todas las lampreas inician su vida como una filtradora larva amoceta, estado en el cual viven por unos cuatro años; en el caso de la lamprea marina tras la metamorfosis nada al mar y vive ahí atacando peces. La lamprea de río en cambio tras la metamorfosis se queda en el río, y no come nunca. Vive 6 mese y tras la reproducción muere sin haber comido jamás: su ventosa oral es mucho menos desarrollada y con menos dientes que la de las lampreas marinas. Las lampreas marinas alcanzan mayor tamaño y viven y comen en el mar por aprox 1-2 años antes de volver a los ríos a reproducirse y morir.


Pero la historia no deja de fascinar. Porque también desde hace mucho que se reconoce un fenómeno de "especies pareadas" tal que existen dos especies hermanas, donde una especie es marina, y la otra, de río. Es decir, no existe un clado de lampreas marinas, y otras de río.
Más aún estudios recientes han observado marcadores genéticos para evaluar el grado de aislamiento en pares de especies mar-río. El impresionate resultado es que no se encontró aislamiento genético alguno, sugiriendo fuertemente hibridización e intercambio de genes. Es decir, la separación entre lampreas marinas y de río corresponden más bien a dos estados de una sóla especie polimórfica.
Un polimorfismo tan drástico ya es fascinante. Cómo se determina el destino en el mar o el río de las lampreas? Sólo sabemos que las lampreas de río colocan huevos más grandes que las de mar, lo que sugiere algún factor ecológico, una "señal" ambiental...ya saben uds...algo epigenético

Referencia:

ESPANHOL R, ALMEIDA PR, y ALVES MJ. 2007 Evolutionary history of lamprey paired species Lampetra fluviatilis (L.) and Lampetra planeri (Bloch) as inferred from mitochondrial DNA variation. Molecular Ecology 16, 1909–1924

Una Historia de Sesgos Perceptuales y Parasitismo...

E aquí un interesante caso del establecimiento y mantención de relaciones interespecificas gracias a las propiedades dinámicas (en este caso sesgos percepuales) de los organismos (ver Saul-Gershenz & Millar 2006):

El “escarabajo de la ampolla” Meloe fransiscanus (Meloidae) parásita como larva los nidos de ciertas abejas y vive en ambientes desérticos de dunares y entre algunas gracias que hace el adulto es toxico y su mordedura genera hinchazones (Tamulinas & Reagor 1979), además presenta ciclos de vida hipermetamorficos (Fig 1), donde algunos estadios larvales pueden o no ocurrir dependiendo de los ambientes que encuentre el organismo en su ontogenia.

Figura 1: Ciclo de vida del escarabajo de la ampolla,
A = adulto, E = huevo, T = 1er estadio o triungulin, FG = 1ra fase de larva,C = fase coarctate en estadios 6 o 7, SG = segunda fase de larva, P = pupa

Las larvas de primer estadio (llamadas tringulines) son muy frágiles y de no encontrarse en un hábitat con abundante alimento y condiciones ambientales propicias mueren rápidamente. La hembra pone su huevo a la base de plantas que crecen en los dunares. Al eclosionar, los tringulines trepan por miles a las puntas de ramas debido a que presentan fototactismo positivo y evaden también el calor de la superficie del suelo. Al trepar en las plantas forman agregaciones de individuos como bolas (Fig 2), lo que se ha sugerido esta relacionado con la prevención de la desecación dada la aridez y dificultad de desplazamiento y disponibilidad de recursos alimenticios como nidos o polen en este ambiente desértico en que habita esta especie.

Figura 2: Masa de tringulines apelotonados y hambrientos..

En este punto la agregación podría considerarse fatalmente condenada a morir si no fuese por que tanto el tamaño como algunos compuestos que componen el olor de esta bola de tringulines atraen al macho de la abeja solitaria Habrodopa pallida (Figura 3) quien se aproxima a la bola confundiéndola por una hembra de su especie...

Figura 3: El incauto macho se aproxima a los tringulines atraido por su forma y perfume..

En este punto la desesperada masa de tringulines se aferran al macho que intenta copular con esta (Figura 4) y, de esta forma, son transportados de esta forma a la hembra de la abeja, a la que se trasladan cuando el macho copula con esta, luego solamente les falta esperar que la abeja regrese a su nido para alimentarse del polen colectado por ella y también del único huevo que depositará…

Figura 4: Foresis de los tringulines a expensas del macho de la abeja solitaria..

Se sabe que la forma de la bola de tringulines no es suficiente para que se establezca la conexión con el macho de la abeja y que el olor analizando los hidrocarbonos cuniculares de los tringulines se parece a algunos presentes en las abejas y que para confundir al macho es necesaria la concentración de estos similar a la emitida por una bola de tringulines agrupados...

Interesante Eh... Eh.. Eh?...

Diablete



Algunas Referencias:

Ray AC, Tamulinas SH, Reagor JC. 1979. High pressure liquid chromatographic determination of cantharidin, using a derivatization method in specimens from animals acutely poisoned by ingestion of blister beetles, Epicauta lemniscata. American Journal of Veterinary Research 40: 498-504.

Saul-Gershenz L S. & Millar J G. (2006) Phoretic nest parasites use sexual deception to obtain transport to their host's nest. PNAS, v 103,n 38, 14039–14044.