Vanessa C. Miller-Sims

Smelling home can prevent dispersal of reef fish larvae

Many marine fish and invertebrates show a dual life history where settled adults produce dispersing larvae. The planktonic nature of the early larval stages suggests a passive dispersal model where ocean currents would quickly cause panmixis over large spatial scales and prevent isolation of populations, a prerequisite for speciation. However, high biodiversity and species abundance in coral reefs contradict this panmixis hypothesis. Although ocean currents are a major force in larval dispersal, recent studies show far greater retention than predicted by advection models. We investigated the role of animal behavior in retention and homing of coral reef fish larvae resulting in two important discoveries: (i) Settling larvae are capable of olfactory discrimination and prefer the odor of their home reef, thereby demonstrating to us that nearby reefs smell different. (ii) Whereas one species showed panmixis as predicted from our advection model, another species showed significant genetic population substructure suggestive of strong homing. Thus, the smell of reefs could allow larvae to choose currents that return them to reefs in general and natal reefs in particular. As a consequence, reef populations can develop genetic differences that might lead to reproductive isolation.

Dispersal in the spiny damselfish, Acanthochromis polyacanthus, a coral reef fish species without a larval pelagic stage

The spiny damselfish, Acanthochromis polyacanthus, is widely distributed throughout the Indo‐Australian archipelago. However, this species lacks a larval dispersal stage and shows genetic differentiation between populations from closely spaced reefs. To investigate the dispersal strategy of this unique species, we used microsatellite markers to determine genetic relatedness at five dispersal scales: within broods of juveniles, between adults within a collection site (~30 m2), between sites on single reefs, between nearby reefs in a reef cluster, and between reef clusters. We sampled broods of juveniles and adults from seven reefs in the Capricorn‐Bunker and Swain groups of the Great Barrier Reef. We found that extra‐pair mating is rare and juveniles remain with their parents until fledged. Adults from single sites are less related than broods but more related than expected by chance. However, there is no evidence of inbreeding suggesting the existence of assortative mating and/or adult migration. Genetic differences were found between all of the reefs tested except between Heron and Sykes reefs, which are separated only by a 2‐km area of shallow water (less than 10 m). There was a strong correlation between genetic distance, geographical distance and water depth. Apparently, under present‐day conditions spiny damselfish populations are connected only between sites of shallow water, through dispersal of adults over short distances. Assuming that dispersal behaviour has not changed, the broad distribution of A. polyacanthus as a species is likely based on historical colonization patterns when reefs were connected by shallow water at times of lower sea levels.

Auditory experience refines cortico-basal ganglia inputs to motor cortex via remapping of single axons during vocal learning in zebra finches

Experience-dependent changes in neural connectivity underlie developmental learning and result in life-long changes in behavior. In songbirds axons from the cortical region LMAN(core) (core region of lateral magnocellular nucleus of anterior nidopallium) convey the output of a basal ganglia circuit necessary for song learning to vocal motor cortex [robust nucleus of the arcopallium (RA)]. This axonal projection undergoes remodeling during the sensitive period for learning to achieve topographic organization. To examine how auditory experience instructs the development of connectivity in this pathway, we compared the morphology of individual LMAN(core)→RA axon arbors in normal juvenile songbirds to those raised in white noise. The spatial extent of axon arbors decreased during the first week of vocal learning, even in the absence of normal auditory experience. During the second week of vocal learning axon arbors of normal birds showed a loss of branches and varicosities; in contrast, experience-deprived birds showed no reduction in branches or varicosities and maintained some arbors in the wrong topographic location. Thus both experience-independent and experience-dependent processes are necessary to establish topographic organization in juvenile birds, which may allow birds to modify their vocal output in a directed manner and match their vocalizations to a tutor song. Many LMAN(core) axons of juvenile birds, but not adults, extended branches into dorsal arcopallium (Ad), a region adjacent to RA that is part of a parallel basal ganglia pathway also necessary for vocal learning. This transient projection provides a point of integration between the two basal ganglia pathways, suggesting that these branches convey corollary discharge signals as birds are actively engaged in learning.

Morphology of axonal projections from the high vocal center to vocal motor cortex in songbirds

Only birds that learn complex vocalizations have telencephalic brain regions that control vocal learning and production, including HVC (high vocal center), a cortical nucleus that encodes vocal motor output in adult songbirds. HVC projects to RA (robust nucleus of the arcopallium), a nucleus in motor cortex that in turn projects topographically onto hindbrain neurons innervating vocal muscles. Individual neurons projecting from HVC to RA (HVCRA) fire sparsely to drive RA activity during song production. To advance understanding of how individual HVC neurons encode production of learned vocalizations, we reconstructed single HVC axons innervating RA in adult male zebra finches. Individual HVCRA axons were not topographically organized within RA: 1) axon arbors of HVC cell bodies located near each other sent branches to different subregions of RA, and 2) branches of single HVC axons terminated in different locations within RA. HVCRA axons also had a simple, sparse morphology, suggesting that a single HVC neuron activates a limited population of postsynaptic RA neurons. These morphological data are consistent with previous work showing that single HVCRA neurons burst sparsely for a brief period of time during the production of a song, indicating that ensembles of HVCRA neurons fire simultaneously to drive small temporal segments of song behavior. We also examined the morphology of axons projecting from HVC to RA cup, a region surrounding RA that receives input from auditory cortex. Axons projecting to RA cup also sent some branches into RA, suggesting direct integration between the sensory and motor circuits for song control. J. Comp. Neurol. 520:2742–2756, 2012.

How stable are the reef odor preferences of settling reef fish larvae

Settlement-stage larvae of the coral reef fishes Ostorhinchus doederleini (Apogonidae) and Pomacentrus coelestis (Pomacentridae) prefer the odor of their settlement reef to that of other nearby reefs. It was unknown whether these olfactory preferences are temporally stable or the result of recent olfactory experience. Ostorhinchus doederleini and P. coelestis larvae were held in aquaria and exposed to water from either their settlement reef or a neighboring reef for 5–9 days and their olfactory preference was tested. We show that exposure to water from another reef did not influence olfactory preference. Ostorhinchus doederleini olfactory preference declined slightly over time whereas P. coelestis preference was gradually lost after 2–3 days in captivity. Neither species switched their preference to the new reef odor. While we cannot determine conclusively the time window of odor learning, imprinting at or shortly after birth is logical and has been demonstrated in other fish species.

Development of auditory-vocal perceptual skills in songbirds.

Songbirds are one of the few groups of animals that learn the sounds used for vocal communication during development. Like humans, songbirds memorize vocal sounds based on auditory experience with vocalizations of adult “tutors”, and then use auditory feedback of self-produced vocalizations to gradually match their motor output to the memory of tutor sounds. In humans, investigations of early vocal learning have focused mainly on perceptual skills of infants, whereas studies of songbirds have focused on measures of vocal production. In order to fully exploit songbirds as a model for human speech, understand the neural basis of learned vocal behavior, and investigate links between vocal perception and production, studies of songbirds must examine both behavioral measures of perception and neural measures of discrimination during development. Here we used behavioral and electrophysiological assays of the ability of songbirds to distinguish vocal calls of varying frequencies at different stages of vocal learning. The results show that neural tuning in auditory cortex mirrors behavioral improvements in the ability to make perceptual distinctions of vocal calls as birds are engaged in vocal learning. Thus, separate measures of neural discrimination and behavioral perception yielded highly similar trends during the course of vocal development. The timing of this improvement in the ability to distinguish vocal sounds correlates with our previous work showing substantial refinement of axonal connectivity in cortico-basal ganglia pathways necessary for vocal learning.