Evolution of Learning Mechanisms in Mollusks

The ability to identify neurons individually can be used within a comparative framework to determine the evolutionary history of the mechanisms underlying habituation, disha-bituation, and sensitization. Suppose that “excitability” and “spike broadening,” two of the mechanisms of response facilitation described previously, are treated as neuromodulatory phenotypes of Aplysia’s mechanosensory neurons. If the phylogenetic relationships among a group of mollusk species were determined independently, could this tell us something about the evolution of these learning mechanisms?

Wright, Kirschman, Rozen, and Maynard (1996) followed a four-step approach to answer this question. First, six species of opistobranch mollusks were selected for analysis (Genera: Bulla, Akera, Aplysia, Dolabella, Bnrsatella, and Dolabrifera). Second, their phylogenetic relationships were determined by morphological characters. Third, sensory neurons homologous to Aplysia’s tail-sensory neurons (stimulated in dishabituation and sensitization experiments) were identified in each species in terms of their location, size, and resting physiology. Finally, the state of the two neuromodulatory characters (presence or absence of serotonin-induced excitability and spike broadening) was determined for each species and mapped into the cladogram (Figure 4.15).

Figure 4.15 Cladistic analysis ot learning mechanisms in mollusks. The phylogenetic tree was obtained by running the program PAUP on a matrix of 12 morphological characters tor the six species. Then, the presence vs. absence of two neuromodulatory traits, spike broadening and increased excitability, was established in homologous mechanosensory neurons in these six species and mapped into the cladogram. Two main results are emphasized: increased excitability evolved before spike broadening, and both mechanisms are lost in Dolabrifera.

Source: Wright, Kirschman, Rozen, and Maynard (1996); reproduced with permission from Evolution.

Two conclusions can be drawn from this phylogenetic analysis. First, increased excitability evolved before spike broadening in these sensory neurons. This is based on the presence of increased excitability and absence of spike broadening in two basal groups: Akera and Bulla. Therefore, serotonin-mediated excitability and spike broadening have evolved independently because some basal genera (Bulla, Akera; Figure 4.15) show the former, but not the latter. This also implies that spike broadening is recently evolved, relative to increased excitability.

Second, both increased excitability and spike broadening have apparently been lost in the tail sensory neurons of Dolabrifera’s recent ancestors since both traits were found in Aplysia, Dolabella, Bursatella, and Phyllaplysia. The absence of these neuromodulatory traits predicts that short-term and long-term sensitization should also be absent in Dolabrtfera, as indeed they are (Wright, 1998). Interestingly, Aplysia and Dolabrtfera exhibit comparable levels of habituation of the mantle-withdrawal response, suggesting that Dolabrtfera is capable of some forms of learning. Consider also the absence of spike broadening in Bulla and Dolabrtfera shown in Figure 4.15. The phylogenetic tree suggests that the absence of spike broadening is a basal or plesiomorphic condition in Bulla, but due to evolutionary reversal in Dolabrtfera.

Sensitization likely evolved as an antipredator mechanism. In fact, individual Aplysia that survived a lobster attack exhibit sustained sensitization relative to undisturbed animals, including increased excitability of sensory neurons (Mason et al., 2014). The absence of sensitization in Dolabrtfera begs the question: how else does this species deal with predators? Apparently, Dolabrtfera evolved a specific pattern of daily activity that tends to avoid predatory encounters (Himstead & Wright, 2018). Most of the day, these tropical mollusks remain inactive, protected under boulders in a tidal pool. When the tide falls below the water level of their pool during the middle of the day, they emerge to forage for food for about one to three hours and then return to their hiding places. It is possible, therefore, that Dolabrtfera has lost the neural mechanisms responsible for sensitization because of its efficient avoidance of predators.

There is a connection between aversive learning (as in sensitization) and predatory encounters that may result in peripheral tissue injury. Most experiments with Aplysia are based on aversive stimuli that activate sensory neurons in the skin (Walters, 1991). These cells are in a prime location to detect life-threatening injury. Skin damage generates sustained discharges from both damaged and surviving sensory neurons in the area of attach during a few seconds following tissue injury. The CNS receives high-frequency discharges much like during sensitization training. This is followed by synaptic facilitation and cellular repair processes that likely involve the growth of axon terminals. Such synaptic facilitation can last for weeks and sensitize reflexes initiated by contact near the injured area. This close parallel between cellular changes following injury and sensitization training suggests an evolutionary connection between these two processes. Learning mechanisms based on nociceptive signals, such as those reviewed in this chapter, may have appeared early in animal evolution and thus be common to many species (Walters, 2018).