Parental Care Usurpation as a model for thinking about Developmental Systems

Parental Care usurpators exploit the social behavior of their hosts, this “modo de vida,” it is present in numerous taxa and involve the partial sequestration of the ontogenetic niche of the host species. In this commentary I will mention two cases of parental care usurpation: the avian brood parasites (e.g. cuckoos) and the ant nest usurpations (often called slave-maker ants or pirate ants).

Due to the very emergent properties involved in the evolution of these life styles; these cases are interesting models for thinking about the value of Developmental System Theory or Evolution by Means of Natural Drift as explanatory backgrounds.

Previously in this blog, we have seen comments about the relevance of the “incomplete isolation” of the multicellulars systems processes as a way to understand certain kinds of dynamic changes in the ontogenetic niche. This “epigenetic permeability”, could be suggested as a property that may help to understand why it is not always necessarily an “Internalization” (i.e incorporation of adaptative traits in the genome of the evolving species) for the development of new life styles or lineage changes in order to get an idea of the points when this “epigenetic permeability” may help to explain the establishment and conservation of these life styles, lets compare the steps of the parasite-host interactions.

In avian brood parasites, the female lays the egg in the host nest, which has been recognized by some authors as the only interaction between the parasite and host species. I would suggest to add a second step that is performed by the parasite chick: the expulsion from the nest of the host offspring (this does not always happen though). For the realization of step one of the interaction, the parasite mother had to find the appropriate host nest and the host parents have to be fooled to keep believing that the extra egg belongs to them. Some parasites species present similar egg pigmentation with their main host, but it is not clear, as far as I´ve read, that this is genetically determined and that this trait can vary inter and intraspecies. The second step is very similar to other kind of parasitic interaction where the allocation of resources is diverted to feed the growing parasite (See Sacculina barnacles post in this blog as an example).

In ant nest usurpation species, the first step involves the usurpation of the queen host throne by the parasite ant. The female searching for nest, sneaking in the nest without being detected as alien by the colony, and (as similar as the avian parasite chick) the diversion towards the reproducing parasite.

In the second step, the parasite queen offspring will search for new host colonies, raid them and kidnap host worker’s larvae. Experiments have demonstrated that when two alternative host are available for the queen and she picks one of them in the first step, the parasite sons will also choose that one for collecting more workers.

This two examples suggest to me that the Developmental System is more than the niche variables and the inheritable organism material, and cannot be reduced to the somatic and germinal part as a satisfactory explanatory background but also the construction of these parasitic life styles due to epigenetic permeability are possible thanks to crucial behavioral operations (“conducta” in Maturana’s approach) that allow the emergence of these very externalized and dependent systems.

Cristian Villagra

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.

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.

El Extraordinario Pato Quetru

Para ilustrar la continuidad de los procesos sistémicos de cambio onto-filogeneticos, podríamos sugerir el enigmático caso del Pato Quetru no Volador (Tachyeres pteneres) en comparación con el Pato Quetru Volador (Tachyeres patachonicus) ambos correspondientes a la Familia: Anatidae Subfamilia: Tadorninae.
Este interesante pato (conocido también como patovapor de Magallanes) se encuentra desde Chiloe al Cabo de Hornos y por Argentina de Chubut a Tierra del Fuego habitando costas rocosas y protegidas. Se alimentan de peces, moluscos y crustáceos que capturan buceado durante la marea alta (De la Peña & Rumboll, 1988). Esta ave tiene la peculiaridad de no volar y ser “sedentario”, lo que se ha atribuido a la longitud de sus alas y a su peso. Similar a esta especie pero más liviano y de alas y colas de mayor tamaño es el pato Quetru volador, que habita simpátricamente a su hermano no volador y tiene una dieta similar. Interesantemente además, este último puede habitar también lagos y lagunas interiores, regresando a la costa estacionalmente. Facultativamente, este pato puede quedarse viviendo en la costa frecuentando los mismos lugares del Quetru no-volador sin migrar a aguas interiores, en este caso se ha descrito que esta especie asimilaría el comportamiento del patovapor de no volar o en caso de emprender vuelo lo hace a último momento bajo este modo de vida, una tabla de comparaciones morfológicas y otros datos puede verse en la pagina web citada en las referencias.
Estudios de genética de poblaciones han encontrado diferencias entre estos patos, donde el pato volador es el mas distinto genéticamente de otra variedades relacionadas, mientras que el patro Quetru volador es mas cercano genéticamente a las especies T. brachypterus y T. leucocephalus (Corbin et al, 1988).
Por otro lado, no solamente es posible encontrar variabilidad genetica y conductual en la especie voladora, estudios de la variación geográfica de la morfología del esqueleto de estos patos coherentes con las reglas ecogeográficas de latitud, pero también presentarían tendencias localidad-especifica en la morfología ósea (Livezey, 1996).
Considerando que la morfología puede ser heredada tan indirectamente como los patrones de movimiento, este caso podría corresponder a un ejemplo de cómo la conducta, es decir la relación creativa del organismo con el medio a través de los modos de vida esta generando cambio evolutivo onto-filogenético. Se podría especular que el pato Quetru no volador es una variante derivada del volador, donde las condiciones de existencia del modo de vida sedentario coincidieron suficientemente como para que la conducta y la morfogia se constituyesen como un sistema heredable. Alternativamente estos patos son el resultado de mutaciones puntuales que a traves de micro y macro seleccion dieron como resultado estas maravillosas adaptaciones...etc etc etc...
Bueno, Pero para saber eso hay que ir al Sure a muestrear!

Diablete

REFERENCIAS:

Kendall W. Corbin, Bradley C. Livezey, Philip S. Humphrey (1988) Genetic Differentiation among Steamer-Ducks (Anatidae: Tachyeres): An Electrophoretic Analysis. The Condor, Vol. 90, pp. 773-781

De la Peña, MR & Rumboll, M (1988) Birds of Southern South America and Antartica.HarperCollins Ed, 304p.

Livezey, BC (1996) Geographic variation in skeletons of flying steamer-ducks (Anatide: Tachyeres patachonicus) Journal of Biogeography, 13, 511-525

y En la Red:
http://www.avesdechile.cl/