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.

One classic “tradeoffs” of sexual reproduction is the risk of acquiring sexual transmitted diseases. But if we now consider that many microbial and viruses associations survive or have been integrated inside the eukaryotic organism (ie “mutualistic”), this allow us to consider sexual contact as a chance to acquire symbiotic associates. In aphids symbiotic bacteria are inherited maternally, this has been demonstrated to be very conservative in parthenogenetic populations. One way to acquire the symbiont is by ingesting it in diets or by microinjections. Alternatively during sexual reproduction, male-borne symbionts can be acquired by females and subsequently transferred to sexually or parthenogenetic generated offspring. This transference is stable trough generations and can establish inheritable acquired characters such as defense towards natural enemies or resistance to heat.


This is the case of the worldwide distributed pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae). In this insect, besides the main Buchnera aphidicola simbiont (that is required for “normal” development and reproduction), other three bacterial symbionts may be present: Candidatus “Hamiltonella defense”, Candidatus “Serratia symbiotica”, and Candidatus “Regiella insecticola” (all members of Enterobacteriaceae). Different aphid population can present from zero to all of those bacterias. Aphids (in their native habitats) usually have all female parthenogenetic reproduction from spring to autumn, then a single generation of sexually reproducing offprings is born (this is related with the shortening of the photoperiod), as a result of copulation these females will lay overwintering eggs and restart the cycle of parthenogenetic reproduction (Fig.1).

Figure 1: Schema of aphid life cycle using A. pisum as example

During copulation, male insects transfer sperm as well as other substances produced from accessory glands. In this, sexually transmitted viruses and bacteria can be transferred to the female. In the case of the pea aphids symbionts present in the male aphid gonads (Fig. 2) R. insecticola can be transferred to the female by the seminal fluid. This has been tested simulating the sexual reproduction season in laboratory strains with and without the different bacterial symbionts and it was demonstrated that copulation between a male carrier with a non infected female can result in a venereal horizontal transmission of the bacterial symbionts! (Moran & Dunbar, 2006).Thus the female and the following parthenogenetic strain generated acquire the symbiotic association.

Interestingly, the acquired association between the aphid and the different Enterobacteriaceae could generate changes in the organism relation with the environment such as the acquired ability to survive parasitoid wasp infections, fungal pathogens, and expansions in the insect niche thanks to acquired ability to use other host plant or to become resistant to a broader range of temperature.
This show again the relevance of understands the organism as a creative onto-phylogenetic dynamic process of development. Better than to focus only on the phenotypic filter as a motor of evolutionary processes.

Figure 2: Localization of the symbionts within the male reproductive system (from Moran & Dunbar, 2006) by using FISH probe matching the 16S rRNA sequence of R. insecticola (green and bright yellow) and with propidium iodide DNA counterstain (red), (Scale bars, 0.1 mm.).

Diablete

References:

Moran NA & Dunbar HE (2006) Sexual acquisition of beneficial symbionts in aphids. PNAS, vol. 103, 34, 12803–12806.