The Light In The Black Box

Adela

In the first chapter of his book Darwin’s Black Box, Michael Behe lays out his fundamental purpose: to show that Darwinian evolution does not account for the molecular structure of life (Behe, 25). He goes on to argue that life depends on many molecular systems that are ‘irreducibly complex’, consisting of interlocking parts that must be all in place before they can function. The need for minimal function would preclude the existence of the constituent parts as they would be useless without one another.

Behe cites the human eye as an example: on top of the structure of the eye itself, the biochemical pathways leading up to the recognition of an image in the brain are ‘staggeringly complicated’ (Behe, 18-22). As an analogy, Behe invokes the mousetrap, which requires a minimum number of interacting parts assembled from the outset to catch any mice at all (Behe, 42-44). By the same token, an irreducibly complex organic system such as the eye must be assembled all at once. Its piece by piece evolution would, according to Behe, involve ‘unbridgeable chasms’ from molecular machine to molecular machine (Behe, 15).

Behe contends that a molecular system is irreducibly complex unless the actions of proteins and other molecules involved can be listed in full detail (Behe, 22). He demands an explanation for how the machinery evolved, but at the same time deems natural selection as insufficient to account for their development (Behe, 27-30). Thus, he attributes the fundamental biochemical pathways of life to intelligent design (Behe, 15).

Behe’s argument is fundamentally flawed. First and foremost, it is based on ignorance. Due to a lack of knowledge on the evolutionary history of molecular pathways, he makes the oversimplistic assumption that it does not exist. Also, Behe tends to focus on the current form-function relationship of molecules in cells, without recognizing that they might not have always have had that one same structure or purpose. Finally, from a scientific perspective, intelligent design is unacceptable because it is unfalsifiable. If the same demands for evidence of irreducible complexity were made of Behe, he too, would have to admit to taking logical flights of fancy in Calvin’s box (Behe, 23).

The very purpose of science is to seek answers to the unknown. And indeed, as more and more information about the actions of proteins and other molecules is discovered, we draw ever nearer to elucidating the origins of biochemical pathways. What Behe fails to recognize is that the opening of the black box is precisely the key to the apparent mysteries of the cell, and of our biochemical origins.

Contrary to the purported ‘eerie and complete silence’ meeting Behe’s demand for explanations of how evolution could have occurred (Behe, 5), the international scientific community has produced, and continues to produce, a wealth of literature regarding this topic. While he scoffs at some earlier work attempting to account for the molecular evolution of the immune system (Behe, 136-137), more evidence in support of these accounts has been uncovered since the initial publication of Darwin’s Black Box in 1996. By closely examining Behe’s critique of the immune system in Chapter 6 of his book, and providing recent and well researched counter-examples, we shall demonstrate exactly why his intelligently designed immune system cannot stand.

Simplifying Selection

The first system Behe describes in chapter 6 is the process of clonal selection, which is how the adaptive immune system detects non-self molecules and initiates a response. Antibodies are initially expressed on B cell surfaces (where they are known as B cell receptors or BCRs), and once they bind to a specific antigen, they initiate a signal cascade via a series of modifications of messenger proteins, which ultimately triggers the transcription of genes involved in B cell activation. The B cell then proliferates and differentiates into a plasma cell, which secretes free antibodies that diffuse throughout the tissues of the host organism and bind the same antigen.

Behe maintains that the process of translating the physical binding of the antibody to the B cell for specific antibody secretion is critically dependent on the membrane-bound antibody, a signal transmitter, and the secreted antibody (Behe, 125). In a world of limited resources, it would be extremely wasteful to have a cell with sub-optimal construction for its purpose. Thus, Behe argues that it would make no sense for a lone antibody to be present without the other two components, since it would hardly be able to fight a pathogenic infection by itself (Behe, 126). However, he is overemphasizing the importance of a structure-form relationship. He assumes that an antibody molecule that is incapable of switching between membrane-bound and secreted forms would be useless, but there exists evidence to the contrary. Antibodies are not the only molecules that undergo gene rearrangement to produce a diverse set of antigen receptors. T cell receptors (TCRs) carry out the same function, but are not secreted. So even if antibodies were initially restricted to the membrane-bound form, and were less efficient at binding antigens, they could still have evolved from a TCR-like gene. The ability to rearrange and the ability to switch forms could evolve in separate steps, with each step offering a selectable advantage. Although TCRs that undergo such somatic diversification have not yet been identified in the two extant orders of jawless vertebrates, several homologs α, β, γ and δ T cell antigen receptor genes are present in cartilaginous fish. It appears as if the organization of their TCR loci and the capacity to undergo junctional diversification is reminiscent of that seen in mammals (Rast et al. 1997). This common general mechanism for receptor diversification (to be elaborated on in the proceeding section) provides a clue as to how the BCR might have evolved from the TCR.

Also, four different genes encoding immunoglobulin (Ig) variable-type domains have been identified in the sea lamprey (Petromyzon marinus), one of which encodes a protein with structural similarities to mammalian VpreB molecules, including the absence of a recognizable transmembrane region, a relatively high proportion of charged amino acids in its C-terminal tail and a distinctive secretion signal peptide (Cannon et al. 2005). This molecule, believed to be the earliest ancestor of the BCR, is proof that animals once survived without the signal transmitting component of the clonal selection system.

It is also possible that the ability to rearrange evolved after the evolution of the alternative splicing pattern, resulting in (rather than as a result of) the ability to switch. This post-splicing switch would require that antigen receptors with a single specificity be effective mediators of immunity. There are several families of innate receptors that do not rearrange, called pattern recognition receptors (PRRs), which can be membrane-bound, secreted, or both, and can mount effective immune responses (Medzhitov and Janeway 1997).

A good example is hemolin, a plasma protein from lepidopteran insects. Its rapid induction to high concentrations in the hemolymph of Manduca sexta larvae and its broad specificity for binding to different types of micro-organisms suggest its role as a PRR that participates in detection and elimination of a variety of lepidopteran pathogens (Yu and Kanost 2002). Significantly, sequence analysis shows that while hemolin is not a precursor to immunoglobulins (the type of Ig-domain it possesses is not found in vertebrates), it is structurally and functionally related to cell-adhesion molecules. This dual function for immune response and cell-adhesion suggests that immune molecules arose from cell-adhesion molecule precursors.

By demonstrating the existence of proteins that do not undergo rearrangement, but are able to switch forms, or that undergo rearrangement without switching forms, Behe’s claim of the need for an ‘irreducible’ clonal selection system for minimal function (Behe, 45) is disproved.

Reconciling Recombination

Next, Behe targets the V(D)J gene recombination system (RS), used by all known jawed vertebrates (gnathosomes) to assemble their antigen receptor genes. T and B lymphocyte progenitors rearrange different sets of prototypic Ig variable (V), diversity (D), and joining (J) gene segments to generate antigen binding regions of their respective T or B cell receptors. These regions are further diversified by the enzymatic addition of nonencoded nucleotides in the joints created during V(D)J assembly. The random nature of this process generates many different receptors for invading pathogens.

Behe holds that three components - genes, signal sequences, and cell - are essential for the the V(D)J RS to generate these millions of antibodies, and that there is no feasible pathway by which the system could evolve (Behe, 131). This, however, is not true. In scoffing at the speculation that “a gene from a bacterium might have luckily been transferred to an animal… the protein coded by the gene could itself rearrange genes… in the animal’s DNA there were signals that were near antibody genes,” (Behe, 137) he grossly underestimates the power of natural selection in stepwise, gradual evolution.

Why, one might ask, would natural selection act on DNA in such a specific manner? What selective forces would be acting on them? The answer lies in a truism from Behe himself: “Threats of aggression can come in all shapes and sizes, so defences have to be versatile.” (Behe, 117) For example, APOBECs, or single-stranded DNA-editing enzymes, are known to cause hypermutation of HIV. In particular, a HIV-encoded virion infectivity factor (Vif) targets APOBEC3G for destruction, causing rapid fixation of mutations that alter amino acids at the protein-protein interface. APOBEC genes have been subject to strong positive selection that appears more ancient than, and is likely only partially caused by, modern lentiviruses (Sawyer et al. 2004). The need for defense against foreign antigens is thus good grounds for RNA and DNA editing in primate genomes.

In addition, there exists in the form of the huge Ig superfamily a breeding ground of potential for genetic rearrangement. Ig domains are extremely versatile and used by TCR, BCR, and major histocompatibility complex (MHC) proteins, invariant activating and inhibiting receptors on natural killer (NK) cells, F_C receptors on phagocytes, and other cell surface molecules that regulate T and B cell interactions with each other and with antigen presenting cells. There exist several well-studied invertebrate immune systems involving Ig domain manipulation that bear remarkable similarity to the V(D)J RS that might shed some light on the mechanisms of how a monomorphic germline receptor gives rise to a somatically variable antigen recognition system.

Amphioxus (Branchiostoma floridae, a cephalochordate representing the most phylogenetically proximal sister group to the vertebrates) expresses variable region-containing chitin binding proteins (VCBPs), which have been implicated in innate immunity against intestinal pathogens. VCBPs possess two tandem V region domains fused to a single, C-terminal chitin-binding domain (CBD), and are structurally closely related to the rearranging antigen-binding receptors of jawed vertebrates. Not only are the constituent VCBP domains prototypic of Igs, VCBP3 has particularly been shown to share structural similarities with the more recently derived antigen receptors in folding and three-layer packing, leading to characteristic dimerization, and creation of advantageous binding properties. In addition, it is suggested that VCBPs or their forerunners are adapted to effecting immune recognition through the clustering of hypervariable residues at the solvent-accessible CBD comprising both V domains. As chitin is a very abundant polymer of N-acetylglucosamine in sea water, it is possible that the CBD of a VCBP can interact with chitin degradation products in ingested seawater and multimerize VCBPs as V region-based immune receptors. Natural selection for hypervariable clusters might then cause stabilization of diversified genes encoding V regions into the germline before the innovation of a basic mechanism of somatic reorganization in vertebrates (Prada 2006).

Somatic variation with individualization of the response can also be seen in the modulation of gene expression via alternative splicing in the fibrinogen related proteins (FREPs) of the freshwater snail (Biomphalaria glabrata). They are made of one or two amino-terminal Ig domains and a carboxyl-terminal fibrinogen domain. Recent studies have shown that these genes are diversified extensively at the genome level in individual animals through both point mutations and recombinatorial processes in somatic tissues. In addition, individual variation of another kind, whether due to gene conversion or some other mechanism, is observed in FREPs where a considerably larger number of sequences can be seen at the somatic level than at the genomic level (Zhang 2004). While it is unlikely that the current V(D)J gene structure arose from a common ancestor shared with FREP-employing protostomes, a completely plausible mechanism of genetic rearrangement occurring separately from somatic variation (that could also apply to the V(D)J RS) has been demonstrated, and may become clearer when other deuterostome genomes are annotated.

Moreover, the recent discovery of variable lymphocyte receptors (VLRs) containing leucine-rich repeat (LRR) modules with highly variable amino acid sequences explains the failure to find molecules of adaptive immunity including Ig-like structures, V(D)J gene segments or MHC genes in surviving jawless vertebrates (agnathans, sister group and nearest living phylogenetic relatives of gnathosomes), despite their displaying adaptive immune responses, such as accelerated rejection of secondary skin allografts, elevated agglutination in response to antigens. The sole VLR gene encodes the signal peptide, parts of the N- and C-terminals, and the invariant stalk region of the receptor. It is flanked by many cassettes encoding one, two or three LRR modules that are randomly incorporated into the germline VLR gene via a multistep assembly, thus creating a repertoire comparable in size to that of antibodies in gnathosomes. LRR modules lack recombinatorial signal sequences; instead, short homology sequences may serve as anchorage sites for assembly, suggesting that gene conversion is a probable mechanism for VLR diversification (Alder 2005).

It is hypothesized that the V(D)J RS arose in ostracoderms (agnathans with dermal skeletons, a gnathosome ancestor (Cooper and Alder 2006). There are two possible pathways by which agnathans and gnathosomes diverged: firstly, VLR RS might have evolved in an ancestor shared only by lampreys and hagfishs, and other agnathans fell prey to pathogen-mediated extinction; secondly, VLR RS might have evolved in an ancestor common to both agnathans and gnathosomes, and V(D)J RS was subsequently acquired, leading to existence of receptors of both self and non-self receptors and mixed lymphocyte activation, thus favoring the loss of either system.

The introduction of the Recombination Activating Gene (RAG) enzyme as a transposase into a VJ gene target appears to be a hallmark of generating Ig-type diversity in jawed vertebrates. Homologs of vertebrate Rag1 and Rag2 have been found in the purple sea urchin (Strongylocentrotus purpuratus, an echinoderm invertebrate). In combination with the apparent absence of V(D)J recombination in echinoderms, this finding strongly suggests that linked Rag1- and Rag2-like genes were already present and functioning in a different capacity in the common ancestor of living deuterostomes, and that their specific role in the adaptive immune system was acquired later in an early jawed vertebrate (Fugmann et al. 2006). The identification of RAG-like genes outside of the context of an adaptive immune system thus supports the hypothesis of transposase-mediated junctional rearrangement, or in other words, a mechanism for incorporation of junctional diversification into the V(D)J RS.

Ultimately, there are sufficient grounds for natural selection, as well as a variety of mechanisms by which it may occur to account for the incipient stages of development of complicated gene recombination systems, and to refute Behe’s claim of irreducable complexity.

Complimenting Complement

Finally, Behe addresses the complement system, which is responsible for opsonization of antigens, initiating phagocytosis, and assembly of the membrane attack complex. It is composed of very intricate pathways, requiring precise sequences of activating molecules and regulation by factor molecules. The absence or malfunction of just one protein would disrupt the cascade and render the system ineffective. One of Behe’s main concerns is the centrality of the C3 molecule in the complement system: without it or the molecules that activate it, the lectin, alternative, and classical pathways would all cease to function (Behe, 135). Yet again Behe’s motif is repeated: the myriad requirements of the structure-function relationship block gradual, Darwinian-style evolution (Behe, 138).

But Behe fails to realize that the current components of the complement cascade might not always have been present, nor have played the same roles that they do today. It turns out that certain parts and functions of the vertebrate complement system were absent in their ancestors, but the presence of ancestral homologous proteins suggests their gradual, stepwise accumulation through evolution.

Urochordates do not have a C2 gene that encodes C3 convertase. Instead, they employ activating enzymes knowns as MASPs, which appear to be related by sequence homology to the C1 enzymes of the classical pathway. Analysis of the human MASP-1/3 gene, which encodes two proteases of the lectin pathway, has revealed alternatively used serine-protease-encoding regions for the gene's two protein products. Phylogenetic studies indicate that one arose by retrotransposition early in vertebrate evolution, and after gene duplication, one of the duplicates lost the downstream serine-protease-encoding region, resulting in a gene of the MASP-2 type. Further gene duplications might have generated the C1r and C1s genes, resulting in the four genes found in humans (Dahl et al. 2001).

The proposed pathway of gene evolution provides a feasible account of how the complement system came to straddle innate and adaptive immunity. By adding components such as C2 and C4 onto the invertebrates' cascade, they retained the lectin pathway, but also linked it to adaptive immunity via employment of immunoglobulins in the classical pathway. It is then possible that the C3 convertase in the vertebrate lectin pathway, C2b, gradually took over the function of the invertebrate MASP, such that now the vertebrate complement system is critically dependent on C2b.

Evidence for ancestral homologs of complement component genes with characteristic domains abounds. They have been found not only in jawed vertebrates but also in jawless fish and non-vertebrate deuterostomes (Zarkadis et al. 2001). The identification of homologues of complement components C3 and factor B in sea urchins is another indication that invertebrates possess a simple complement system homologous to the alternative pathway in higher vertebrates (Smith et al. 1998). Also, studies of the crystal structures of native C3 and its final major proteolytic fragment C3c have revealed thirteen domains, nine of which were unpredicted, suggesting that the proteins of the α2-macroglobulin family evolved from a core of eight homologous domains in vertebrate ancestors (Janssen et al. 2005).

Behe defines an irreducibly complex system as one that “cannot be produced gradually by slight, successive modifications of a precursor system, since any precursor to an irreducibly complex system is by definition nonfunctional”. The complement cascade has been shown to be composed of several parts that came to be integrated together in jawed vertebrates, belying Behe's claim and proving that the complement pathways do not present a challenge to step-by-step evolution, but rather, a fitting tribute.

“Rome was not built in a day”; neither were the highly specialized proteins involved in immunity. Having examined the systems of clonal selection, Ig gene recombination and complement in some detail, we have hopefully arrived at a better understanding of how the various components of the immune system might have evolved to work in tandem. Evidently, in contrast to Behe’s claims, the complexity of life’s foundation has hardly ‘paralyzed science’s attempt to account for it’ (Behe, 5), but rather, has spurred on much research, which every day is providing more knowledge about the intricate, but definitely not irreducible, molecular intricacies of life; and will, ultimately, uncover the light at the bottom of the big black box.

REFERENCES

M. J. Behe. 2006.Darwin's Black Box. 10th anniv. ed. New York: Free Press.

J. P. Rast, M. K. Anderson, S. J. Strong, et al. 1997. α, β, γ and δ T cell antigen receptor genes arose early in vertebrate phylogeny. Immunity 6:1–11.

John P. Cannon, Robert N. Haire, Zeev Pancer, M. Gail Mueller, Diana Skapura, Max D. Cooper and Gary W. Litman. Variable domains and a VpreB-like molecule are present in a jawless vertebrate. 2005. Immunogenetics Volume 56, Number 12.

R. Medzhitov, C. A. Jr. Janeway. 1997. Innate immunity: the virtues of a nonclonal system of recognition. Cell 3:295-8.

Xiao-Qiang Yu and Michael R. Kanost. Binding of hemolin to bacterial lipopolysaccharide and lipoteichoic acid. 2002. Eur. J. Biochem. 269:1827-1834.

S. L. Sawyer, M. Emerman, H. S. Malik. Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. 2004. PLoS Biol. 2(9):E275.

José A Hernández Prada, Robert N Haire, Marc Allaire, Jean Jakoncic, Vivian Stojanoff, John P Cannon, Gary W Litman & David A Ostrov. 2006. Ancient evolutionary origin of diversified variable regions demonstrated by crystal structures of an immune-type receptor in amphioxus. Nature Immunology 7:875-882.

Si-Ming Zhang, Coen M. Adema, Thomas B. Kepler, Eric S. Loker. 2004. Diversification of Ig Superfamily Genes in an Invertebrate. Science 305:251-254.

Matthew N. Alder, Igor B. Rogozin, Lakshminarayan M. Iyer, Galina V. Glazko, Max D. Cooper, Zeev Pancer. 2005. Diversity and Function of Adaptive Immune Receptors in a Jawless Vertebrate. Science 310:1970–1973.

Sebastian D. Fugmann, Cynthia Messier, Laura A. Novack, R. Andrew Cameron, and Jonathan P. Rast. 2006. An ancient evolutionary origin of the Rag1/2 gene locus. PNAS Vol. 103 10:3728-3733.

I. K. Zarkadis, D. Mastellos, J. D. Lambris. Phylogenetic aspects of the complement system. 2001. Dev Comp Immunol. 25(8-9):745-62.

L. C.Smith, C. S. Shih, S. G. Dachenhausen. 1998. Coelomocytes express SpBf, a homologue of factor B, the second component in the sea urchin complement system. J Immunol. 161(12):6784-93.

Bert J. C. Janssen, Eric G. Huizinga, Hans C. A. Raaijmakers, Anja Roos, Mohamed R. Daha, Kristina Nilsson-Ekdahl , Bo Nilsson and Piet Gros. 2005. Structures of complement component C3 provide insights into the function and evolution of immunity. Nature 437:505-511.

Masaru Nonaka, Fumiko Yoshizaki. 2004. Primitive complement system of invertebrates. Immunological Reviews Vol. 198: 203.

M. R. Dahl, S. Thiel, M. Matsushita, T. Fujita, A. C.Willis, T. Christensen, T. Vorup-Jensen, J. C. 2001. MASP-3 and its association with distinct complexes of the mannan-binding lectin complement activation pathway. Jensenius. Immunity 15(1):127-35.

So Long and Thanks for All (Your) Fish

Adela

I. BACKGROUND/ THE QUESTION

Dolphins (Delphinidae) are part of a group known as the Odontoceti, which forms a suborder of the cetaceans. As their name suggests, Odontocetes are characterised by having teeth (as opposed to baleen whales in the other suborder of cetaceans, Mysticeti). Toothed whales are active hunters, feeding mainly on fish and squid.

Odontocetes vary considerably in size and morphology. Delphinidae alone vary in size from 1.2 metres and 40 kilograms (Heaviside's Dolphin, Cephalorhynchus heavisidii) to 7 metres and 4.5 tonnes (Orca, Orcinus orca). Teeth may be numerous, with some dolphins bearing over 100 teeth in their jaws; while at the other extreme are the Narwhal (Monodon monoceros) with its single long tusk, and the almost toothless beaked whales (family Ziphiidae).

Odontocetes have a single blowhole on the top of the head, which is used to produce vocalizations. They maintain a broad variety of calls to communicate, but are also capable of using ultrasound for echolocation. As an adaptation for their echolocation, odontocete skulls have become asymmetric, and their brains have increased in size.

Dolphins generally live in groups of up to a dozen animals. These groups, called pods or schools, occasionally merge to form "superpods", aggregations of up to thousands of whales. The complex social relations and high potential for learning of dolphins has led to their being considered being among the most intelligent of animals.

However, dolphins have often been observed to display altruistic behaviour towards schoolmates and even members of other species of odontocetes. Is there sufficient evidence to claim reciprocal altruism (or is it just some form of nepotism at work)? Does such behaviour fit in with selection theory, i.e. is it an evolutionary adaptation? If yes, how so? What are the implications of these findings?

II.YOU SCRATCH MY BACK… / EVIDENCE OF ALTRUISTIC BEHAVIOUR

A. Cooperative feeding

The first and most obvious form of altruistic behaviour would be cooperative feeding. Certain species of dolphins have been observed to swim in certain patterns to herd their prey. For example, the dusky dolphins of Argentina form tight circles around anchovies, paralysing them (possibly by inducing a hypoxic state due to crowding, or by debilitation via intense ensonification) before allowing a member of the pod to rush in for the kill (Booth 1988). This is immensely useful since dolphin prey, such as mahimahi, are typically much swifter in burst speed than dolphins.

In addition, there have been sightings of false killer whales and roughtooth dolphins feeding, in which one individual held a large prey in its jaws and allowed other dolphins to pull off piece of flesh. The prey was passed around from dolphin to dolphin, allowing every individual equal chances of feeding (Brower and Curtsinger 1979). Such food-sharing is evidently not typical behaviour to maximise survival in food-scarce situations.

B. Care-giving

Secondly, dolphins exhibit extended care for each other throughout their lives. Booth (1988) reports that in bottle-nosed dolphins, parental care is often carried out over a lengthy period, with offspring remaining highly dependent on the mother for up to four years (until the calf is weaned). Mothers often form ‘playpens’, in which all their offspring swim protected from predators. They have also been known to ‘babysit’ for each other when they leave the pod for short periods (though in many cases, these females are related and could merely be practising kin selection to improve inclusive fitness).

Dolphins also assist in birthing. Severe teeth marks concentrated on the posterior body and tail flukes of stillborn calves indicate attempts to pull them from the mother (Connor and Norris 1982).

There also exist various other forms of mutual assistance toward injured or distressed animals, under the broad heading of epimeletic behaviour:(a) Standing by occurs when an animal or animals stays with another animal in distress without offering any apparent aid. It involves remaining in dangerous situations for far longer than would be the case with no distressed animal. Odontocetes, from dolphins to sperm whales, will sometimes ‘stand by’ captive dolphins, circling and swimming near the captive vessel (Connor and Norris 1982). I would call this the odontocete equivalent of ‘moral support’.(b) Excitement includes approaching an injured comrade and displaying violent or excited behaviour, such as pressing against and biting restraining lines, propelling injured animals away from captors, or attacking when young animals of the pod are disturbed. For instance, Norris and Prescott (1961) report a case where a shot pilot whale was drifting in rigor mortis toward the capture vessel when two other pilot whales submerged it and took it away. (c) Support involves an animal pressing another to the surface to help it breathe. It is most common intraspecifically, but has also been observed among members of different species. A most dramatic example of this would be that recorded by Siebenaler and Caldwell (1956), in which two bottlenose dolphins buoyed a third which had been stunned by a freak explosion at sea. They had to leave the injured party’s side to breathe but kept returning until it had recovered. In addition, the remainder of the dolphins’ pod remained ‘standing by’ as described above.

C. Mating alliances

Connor and Norris (1982) noted that pairings of juvenile and adult bottlenose males existed within pods. Such pairings existed to protect each other from predation, and to cooperate in hunting and in sexual herding. Male dolphins were observed to operate in pairs and triplets to sequester and control the movements of females. They preferentially herded non-pregnant females likely to be in estrus. Each alliance associated preferentially with one or two other alliances. Occasionally, two alliances combined and took females from another alliance or defended females against such efforts (Connor et al. 1992). Bottlenose dolphins are one of only a few mammalian taxa where the males are known to cooperate within their social group in order to maintain mating access to single females against other males. Male bonds in bottlenose dolphins have been hypothesised as evolving through kinship and associated inclusive fitness effects (Krutzen et al. 2003).

III. THE REAL PLOT/ EXPLANATORY MODELS

Several models have been suggested to explain the unlikely behaviour of dolphins and other odontocetes described above. As Brader and Wursig (1994) put it, “Group size and structure are guided by an incompletely understood matrix of factors, including foraging type, need for predator detection and avoidance, social and sexual interactions, and the care and maintenance of developing young”. They propose that dolphins who coordinate activities in efficiently sized groups benefit by enhanced fitness to themselves and their offspring. Connor and Richards (2001), on the other hand, believe that reciprocal altruism is the agent at work within dolphin societies.

Trivers (1971) stated that the conditions necessary for the evolution of reciprocal altruism are identical to those for kin selection (except that the recipient of an altruistic act need not be related to the actor). We must thus consider the possibility that the entire range of altruistic behaviour is a product of kin selection and that reciprocity does not exist in dolphin societies. Kin selection, also known as kin-directed altruism or nepotism, can be discriminatory or non-discriminatory, depending on the cost of typical altruistic acts to the donor, the benefit to the receiver, and the relatedness of the two parties.

A. Non-discriminatory nepotism

Non-discriminatory nepotism is by far the most commonly offered explanation of dolphin altruism. This explanation attributes helpful behaviour amongst individuals to an “innate behavioral repertoire” of the species that manifests in stereotyped responses to the distress of companions. The innate tendency to rescue offspring and relatives contributes greatly to inclusive fitness and is likely to have been fixed in the species.

However, the model non-discriminatory nepotism has also met with much opposition. The counter-argument provided by Connor and Norris (1982) is that dolphin behaviour is governed much more by learning than by innate patterns. Dolphins are capable of deuterolearning (second order learning, i.e., understanding how different domains of communication operate) – for example, roughtooth dolphins (Steno bredanensis) in captivity quickly made the logical connection between novel jumps and food incentives (Pryor et al. 1969). Innate tendency is thus not a convincing argument for giving aid to others.

Furthermore, epimeletic behaviour is spontaneous and tailored to individual situations. In the rescue of the dead pilot whale (Part II. B. (b)), its body was not supported in a stereotypical fashion but rather taken away from would-be captors in a manner opposite to that of supportive behaviour.

Finally, the discriminatory nepotism model has been refuted by numerous reports of interspecific and even intergeneric assistance behaviour, even between species that are strikingly different morphologically, and thus could not be phenotypically misidentified as kin (precluding the possibility of kin selection).

B. Discriminatory nepotism

Under a system of discriminatory nepotism, an animal will give assistance according to how much it values the recipient’s fitness in relation to its own, given their relatedness in a certain situation. Discriminatory nepotism has already been clearly observed in infant pigtail macaques, with siblings never before seen (Silk 1992).

Smaller dolphins in general have extremely fluid social structures. In fact, perhaps the most significant finding from several studies on the social lives of dolphins is that they form “fusion-fission” societies, in which individuals may join temporary parties of varying sizes, instead of operating in a fixed group (Booth, 1988). If dolphin relations were regulated by discriminatory nepotism alone, we would expect low group fluidity, since a dolphin would consistently prefer to assist more closely related animals than more distantly related animals. Merely swimming with a group of more closely related individuals would represent an increase in inclusive fitness (Connor and Norris 1982). Thus, the model of discriminatory nepotism is not entirely convincing as an explanation for mutual assistance in dolphins either.

C. Reciprocal altruism

Reciprocal altruism is a phenomenon in which one organism provides benefit to another in the expectation of future reciprocation. It usually evolves in the presence of a mechanism to identify and punish "cheaters". However, under this ‘two-party’ model of reciprocal altruism, while there is ample time for dolphins to discover the cheating tendencies of others, consistent ousting of ‘cheaters’ has not been observed; furthermore, it is difficult to account for all cases of interspecific and intergeneric aid, since it requires that aid be given in anticipation of reciprocity specifically from the assisted individual.

The best explanation of epimeletic behaviour in dolphins appears to be a multiparty model of reciprocal altruism, in which altruistic acts are dispensed freely and not only to animals that are expected to reciprocate. Since reciprocal altruism is mediated by learning (i.e., functions independently of genetic relatedness), it explains interspecific epimeletic behaviour, as well as its unpredictable occurrence in dolphins (Connor and Norris 1982).

This model is also consistent with the group fluidity found within some species of dolphins. Group fluidity is based upon the ability to recognise individuals. The more individuals an animal can recognise outside one level of kin association, the higher the potential for altruistic relationships, since animals can then efficiently aggregate appropriate numbers for different activities such as travel, feeding, and socialising. As we already know, dolphins employ a system of calls (blowhole sounds) and imitation to communicate. Playback experiments (Sayigh et al. 1998) have proved dolphins’ capacity for individual recognition (via distinctive signature whistles) and motivation to respond, providing evidence for reciprocal altruism.

Recent studies (e.g., Möller 2001) have found that associations and alliance membership in male dolphins are not associated with either maternal kinship or genetic relatedness; the majority of male pairs within alliances are randomly related, although high relatedness values exist between males of different alliances in the resident population. These findings indicate that mechanisms other than kin selection may be foremost in the development and maintenance of cooperation between male bottlenose dolphins.

Furthermore, herding can explain why males travel in pairs or trios, but if they are competing for females, relationships between the males should be extremely hostile. Connor (2001) points out that on the contrary, alliance members associate with one another consistently even when not herding females, and a great deal of play and stroking occurs in these alliances, indicating that these alliances were not purely utilitarian.

IV. TAKING OVER THE WORLD/ QUESTIONS & IMPLICATIONS

Despite the strong evidence and arguments for reciprocal altruism, there remain several ambiguities and questions to be answered regarding the nature and findings of the research.

Firstly, it is notoriously difficult to observe cetacean activity. Since most observations were carried out on boats, researchers were able to report only events that happened near the surface, and even those were clear only when the water was not choppy (Wursig 1989). Research on dolphin vocalizations is also hindered due to the difficulties of localising sound underwater (Connor 2001).

Secondly, it is possible that small, possibly stable relations based on kinship could be undiscovered due to the small number of animals marked in studies (Connor and Norris 1982). The degree of relatedness between two individuals is also affected by migration, making it difficult to weigh factors against each other and determine if kin selection is operating or not (Hamilton, 1975). Of course, some argue that the scattered and often anecdotal literature on dolphins still adds up to considerable evidence for reciprocal altruism.

One area of curiosity is that seals and sea lions (pinnipeds), which like the odontocetes are carnivorous marine animals, exhibit much less flexible behaviour. Connor and Norris (1982) postulate that the birth and early nurture of dolphins at sea (as opposed to land births in pinnipeds) exposes them to higher predation and accelerates evolution of strategies for sheltering young.

There is also difficulty explaining the phenomenon of mass stranding in larger, polygynous species such as the false killer whale. In a case reported by Caldwell (1970), only one whale out of fifteen was seriously injured, and the others were sufficiently submerged that they could swim away, but they did not. Such behaviour does not confer higher fitness onto any party, nor does it fit any of the models examined so far. The explanation commonly given by proponents of the reciprocal altruism model is that polygyny creates such strong social bonds that a “one-for-all, all-for-one” mentality develops. Other parties such as Morimitsu et al. (1986) proposed that a parasite was responsible for causing a form of cranial nerve damage akin to meningitis that forced them to (fatally) enter shallow waters to respire more easily. However this theory has been met with skepticism as it seemed highly unlikely that the parasite would cause beaching numbering in the hundreds at a time. Larger sample sizes of brain autopsies need to be taken before any definitive conclusions may be reached about air sinus parasitism and its degree of pathology on dolphins.

The recent discovery of multi-level alliances amongst male dolphins (Connor, 2003) serves to complicate the model of reciprocal altruism. Apparently, males in stable first-order or derived second-order alliances are often strongly related so they gain inclusive fitness from alliance membership; while members of ‘superalliances’ (groups of about 14 individuals with highly labile pairs and trios) were related purely by chance. Furthermore, the strength of the association of alliance partners within the super-alliance, as measured by an index of joint participation in consorting a female, was not correlated with genetic relatedness. Thus, within one population and one sex, it appears that there may be simultaneous operation of more than one mode of group formation.

In any case, if dolphins do employ reciprocal altruism, they will be following in the footsteps of other ‘higher mammals’ such as humans and chimpanzees. This agrees with Connor and Norris’ assertion that selection for features of sociality (as exemplified by altruistic behaviour) has major evolutionary linkage with reciprocal altruism. Heavy predation has, perhaps, produced strong selection pressure to practice mutual assistance with higher sophistication, leading to the development of complicated social systems, with ethics not necessarily based on true kinship, but subject to cultural evolution.


V. REFERENCES

Richard C. Connor; Kenneth S. Norris. Are Dolphins Reciprocal Altruists? The American Naturalist, Vol. 119, No. 3. (Mar., 1982), pp. 358-374.

William Booth. The Social Lives of Dolphins. Science, New Series, Vol. 240, No. 4857. (Jun. 3, 1988), pp. 1273-1274.

J. B. Siebenaler; David K. Caldwell. Cooperation among Adult Dolphins. Journal of Mammalogy, Vol. 37, No. 1. (Feb., 1956), pp. 126-128.

Richard C. Connor; Rachel A. Smolker; Andrew F. Richards. Two Levels of Alliance Formation Among Male Bottlenose Dolphins (Tursiops sp.). Proceedings of the National Academy of Sciences of the United States of America, Vol. 89, No. 3. (Feb. 1, 1992), pp. 987-990.

Connor, R.C. Social relationships in a big - brained aquatic mammal. Model Systems in Behavioral Ecology (ed. L.A. Dugatkin). Princeton University Press, Princeton, 2001.

Luciana M. Möller; Luciano B. Beheregaray; Robert G. Harcourt; Michael Krützen. Alliance membership and kinship in wild male bottlenose dolphins (Tursiops aduncus) of southeastern Australia. Proceedings of the Royal Society B: Biological Sciences, Volume 268, Number 1479 / September 22, 2001.

Michael Krützen; William B. Sherwin; Richard C. Connor; Lynne M. Barré; Tom Van de Casteele; Janet Mann; Robert Brooks. Contrasting relatedness patterns in bottlenose dolphins (Tursiops sp.) with different alliance strategies. Proceedings of the Royal Society B: Biological Sciences, Volume 270, Number 1514 / March 07, 2003, pp. 497 – 502.

Stefan Bräger; Bernd Würsig; Alejandro Acevedo; Thomas Henningsen. Association Patterns of Bottlenose Dolphins (Tursiops truncatus) in Galveston Bay, Texas. Journal of Mammalogy, Vol. 75, No. 2. (May, 1994), pp. 431-437.

Laela S. Sayigh; Peter L. Tyack; Randall S. Wells; Andrew R. Solow; Michael D. Scott; A. B. Irvine. Individual recognition in wild bottlenose dolphins: a field test using playback experiments. Animal Behaviour, 1998, 57, pp. 41–50.

David K. Caldwell; Melba C. Caldwell; Cecil M. Walker, Jr. Mass and Individual Strandings of False Killer Whales, Pseudorca crassidens, in Florida. Journal of Mammalogy, Vol. 51, No. 3. (Aug., 1970), pp. 634-636.

Tamotsu Morimitsu; Tomoyuki Nagai; Minoru Ide; Akira Ishii; Masashi Koono. Parasitogenic Octavus Neuropathy as a Cause of Mass Stranding of Odontoceti. The Journal of Parasitology, Vol. 72, No. 3. (Jun., 1986), pp. 469-472.

Joan B. Silk. The Patterning of Intervention among Male Bonnet Macaques: Reciprocity, Revenge, and Loyalty. Current Anthropology, Vol. 33, No. 3. (Jun., 1992), pp. 318-325.

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