Neural mechanisms underlying the evolvability of behaviour

Abstract

The complexity of nervous systems alters the evolvability of behaviour. Complex nervous systems are phylogenetically constrained; nevertheless particular species-specific behaviours have repeatedly evolved, suggesting a predisposition towards those behaviours. Independently evolved behaviours in animals that share a common neural architecture are generally produced by homologous neural structures, homologous neural pathways and even in the case of some invertebrates, homologous identified neurons. Such parallel evolution has been documented in the chromatic sensitivity of visual systems, motor behaviours and complex social behaviours such as pair-bonding. The appearance of homoplasious behaviours produced by homologous neural substrates suggests that there might be features of these nervous systems that favoured the repeated evolution of particular behaviours. Neuromodulation may be one such feature because it allows anatomically defined neural circuitry to be re-purposed. The developmental, genetic and physiological mechanisms that contribute to nervous system complexity may also bias the evolution of behaviour, thereby affecting the evolvability of species-specific behaviour.

Figure 1.

Parallel evolution of long-wavelength photopigments in butterflies and moths. (a) Dendrogram showing parallel evolution of opsins that absorb long-wavelength light. The numbers in parentheses after the species names represent the maximum absorbance wavelength (in nanometres). Both Apodemia mormo (LWRh2) and Papilio xuthus (PxRh3) are significantly red-shifted with respect to other pigments. The shift occurred independently as intermediate pigments show absorbance at shorter wavelengths. (b) Alignment of partial coding sequences for lepidopteran opsins. Identical amino acid substitutions occurred in positions 10, 23 and 29 of transmembrane domain no. 1 (TM1) for Apodemia mormo (LWRh2) and Papilio xuthus (PxRh3) (adapted from Frentiu et al. [44]).

Figure 2.

Homologous identified neurons in sea slugs have divergent or similar roles in behaviour. (a) Tritonia diomedea swims by flexing its body in the dorsal and ventral directions as shown in the diagram to the left. Simultaneous intracellular microelectrode recordings from DSI and C2, two neurons in the central pattern generator (CPG) for the swimming behaviour, display rhythmic bursts of action potentials after a body wall nerve is electrically stimulated (nerve stim.). This comprises the swim motor pattern. (b) The swim CPG in Tritonia contains three neuronal types: DSI, C2 and VSI. There are three DSIs: DSI-A, DSI-B, DSI-C. They are being grouped together for simplicity. The triangles represent excitatory synapses, the circles represent inhibitory synapses and multicomponent synapses are presented by combinations of the two. (c) The swim CPG in Pleurobranchaea has many similarities to that in Tritonia. As1–3 are homologous to the DSIs in Tritonia. There is an As4 that is in the same cell cluster and is in the swim CPG, but is not homologous to the DSIs. Its homologue exists in Tritonia, but the function of this neuron has not been determined in Tritonia. The I_VS neuron has not been identified, but its synaptic actions, which can be inferred from recordings of the other neurons, are similar to those of the Tritonia VSI. A1 (which is homologous to C2 in Tritonia) is strongly electrically coupled to neuron A10 and so both are represented together. Homologues of A3 and A10 have not been identified in Tritonia. (d) Pleurobranchaea californica swims with dorsal–ventral body flexions. Intracellular recordings show that the As2,3 neurons and the A1 neuron both exhibit bursting behaviour during the swim motor pattern (adapted from [109], American Physiological Society, with permission). (e) Melibe leonina swims by flexing its body from side-to-side. Intracellular recordings from CeSP (which is homologous to the DSI in Tritonia) and swim interneuron 1 (Si1) show that the CeSP neuron is not rhythmically active during the swim motor pattern.

Figure 3.

Phylogeny of the Nudipleura based on both anatomical and molecular data [,–118]. The phylogenetic tree shows selected genera and their swimming behaviours. DV (green), dorsal–ventral flexion; L (blue), lateral flexion; N (red), non-swimming.

Figure 4.

(a) Comparison of vasopressin 1a (V1a) receptor distribution in the brains of six mammalian species. The species in the left column display monogamous behaviour and those in the right column are non-monogamous. The arrows in monogamous species point to the high level of expression in the ventral pallidum (VP). The boxes show the lack of staining in this region in non-monogamous species. Images provided by Larry Young. (b) A schematic of the reward circuitry, which is common to rodents. Dopamine (green) from the ventral tegmental area (VTA) is released in the prefrontal cortex (PFC) and the nucleus accumbens (NAcc). The NAcc also receives excitation from the periaqueductal grey (PAG) and nucleus tractus solitarus (NTS), which are activated during sex. The NAcc projects to the ventral pallidum (VP), which is the major output relay that helps reinforce motor behaviour. The medial amygdala (MeA), which gets input from the olfactory bulb (OB), projects fibres to the VP that contain vasopressin (magenta). Differences in the level of V1a receptor expression in VP can modulate the reinforcement of mate-related odours (based upon Young & Wang [159] and Young et al. [160]).