Andries Ter Maat

Coolidge effect in pond snails: male motivation in a simultaneous hermaphrodite.

BackgroundThe simultaneously hermaphroditic pond snail, Lymnaea stagnalis, can mate in the male and female role, but within one copulation only one sexual role is performed at a time. Previous work has shown that male motivation is determined by the availability of seminal fluid in the prostate gland, which is detected via a nervous connection by the brain area controlling male behaviour. Based on this knowledge, patterns of sexual role alternations within mating pairs can be explained.ResultsThe data presented here reveal that these snails can donate and receive sperm several times within 24 hours, and that they have increased mating rates in larger groups (i.e. more mating opportunities). For mating pairs we show, by introducing novel mating partners after copulation, that animals do inseminate new partners, while they are no longer motivated to inseminate their original partners.ConclusionOur findings provide the first direct evidence for higher motivation in a hermaphrodite to copulate when a new partner is encountered. This Coolidge effect seems to be attenuated when mucus trails are excluded, which suggests that a chemical or textural cue may be responsible for mediating this response to sperm competition.

Male accessory gland protein reduces egg laying in a simultaneous hermaphrodite.

Seminal fluid is an important part of the ejaculate of internally fertilizing animals. This fluid contains substances that nourish and activate sperm for successful fertilization. Additionally, it contains components that influence female physiology to further enhance fertilization success of the sperm donor, possibly beyond the recipients optimum. Although evidence for such substances abounds, few studies have unraveled their identities, and focus has been exclusively on separate-sex species. We present the first detailed study into the seminal fluid composition of a hermaphrodite (Lymnaea stagnalis). Eight novel peptides and proteins were identified from the seminal-fluid-producing prostate gland and tested for effects on oviposition, hatching and consumption. The gene for the protein found to suppress egg mass production, Ovipostatin, was sequenced, thereby providing the first fully-characterized seminal fluid substance in a simultaneous hermaphrodite. Thus, seminal fluid peptides and proteins have evolved and can play a crucial role in sexual selection even when the sexes are combined.

Aspects of body size and mate choice in the simultaneously hermaphroditic pond snail Lymnaea stagnalis.

Body size can be a good indicator of the quality of a potential mate in terms of fecundity. In many hermaphrodites, egg production is positively correlated with body size. Especially when donating sperm is costly, a preference for larger partners might be expected. Here we test this prediction for the great pond snail Lymnaea stagnalis. As expected, we find a clear effect of body size on egg production, and show that shell height can be used as a reliable predictor of body size. Additionally, behavioural observations reveal that these snails are not physically limited in mating with a much larger or smaller partner. Nonetheless, both in a choice experiment as well as in spontaneous copulations, we find no evidence of mate choice based on body size. These results contribute to a growing field of research which attempts to understand the evolution of the wide variation in the ways that hermaphroditic species respond to the size of potential mating partners.

Zebra finch mates use their forebrain song system in unlearned call communication.

Unlearned calls are produced by all birds whereas learned songs are only found in three avian taxa, most notably in songbirds. The neural basis for song learning and production is formed by interconnected song nuclei: the song control system. In addition to song, zebra finches produce large numbers of soft, unlearned calls, among which “stack” calls are uttered frequently. To determine unequivocally the calls produced by each member of a group, we mounted miniature wireless microphones on each zebra finch. We find that group living paired males and females communicate using bilateral stack calling. To investigate the role of the song control system in call-based male female communication, we recorded the electrical activity in a premotor nucleus of the song control system in freely behaving male birds. The unique combination of acoustic monitoring together with wireless brain recording of individual zebra finches in groups shows that the neuronal activity of the song system correlates with the production of unlearned stack calls. The results suggest that the song system evolved from a brain circuit controlling simple unlearned calls to a system capable of producing acoustically rich, learned vocalizations.

Spontaneous and induced egg laying behavior of the pond snail lymnaea-stagnalis

SummaryInLymnaea egg laying is initiated by the discharge of the neurosecretory caudodorsal cells (CDCs), which release an ovulatory hormone (caudodorsal cell hormone; CDCH) and other peptides. Egg laying is a complex behavioral pattern composed of various postures and action patterns. This paper describes the egg laying behavior of intact and freely behaving animals as it occurs spontaneously after an environmental stimulus (clean water stimulus; CWS), and following injections of highly purified CDCH. CDC discharges were monitored in vivo with chronically implanted electrodes. In these animals the egg laying behavior following spontaneous and electrically elicited CDC discharges was analyzed.1.The egg laying behavior induced by the CWS consisted of three separate phases that occurred in a fixed temporal sequence. Shortly after transferral to clean water, animals became quiescent (resting). This was followed by an active phase (turning) during which behaviors were performed to prepare the substrate for the subsequent oviposition phase. Following oviposition, animals examined the deposited egg mass.2.After spontaneous CDC discharges and CDC discharges elicited by selective electrical stimulation of the CDCs (with a chronically implanted fine wire electrode) the egg laying behavior was the same as that following the CWS. All phases of egg laying behavior followed the CDC discharge.3.In contrast, the egg laying behavior following injections of highly purified CDCH was different to that following the CWS. These animals showed no resting phase. Instead, they continued locomoting and entered directly into the turning phase. The animals that did not lay eggs after injection because they were refractory did not show egg laying behavior.4.The durations of the joint turning and oviposition phases depended strongly on clutch size, suggesting that the ovulated eggs are instrumental in causing this behavior.5.We conclude that whenever egg laying is preceded by a CDC discharge, either occurring spontaneously or induced by CWS or electrical stimulation, the behavior differs from that following injections of CDCH directly into the blood. This demonstrates that the presence of CDCH in the blood is not sufficient to produce the full complement of egg laying behaviors and suggests that CDCH, or one of the other peptides released during a CDC discharge, has important local effects within the CNS.

Patterns of call communication between group-housed zebra finches change during the breeding cycle

Vocal signals such as calls play a crucial role for survival and successful reproduction, especially in group-living animals. However, call interactions and call dynamics within groups remain largely unexplored because their relation to relevant contexts or life-history stages could not be studied with individual-level resolution. Using on-bird microphone transmitters, we recorded the vocalisations of individual zebra finches (Taeniopygia guttata) behaving freely in social groups, while females and males previously unknown to each other passed through different stages of the breeding cycle. As birds formed pairs and shifted their reproductive status, their call repertoire composition changed. The recordings revealed that calls occurred non-randomly in fine-tuned vocal interactions and decreased within groups while pair-specific patterns emerged. Call-type combinations of vocal interactions changed within pairs and were associated with successful egg-laying, highlighting a potential fitness relevance of calling dynamics in communication systems. DOI: http://dx.doi.org/10.7554/eLife.07770.001

Effects of age, size, and mating history on sex role decision of a simultaneous hermaphrodite

Lay summary Quite a few animals are male and female at the same time, so they can choose to mate either as male or female on copulation. The decision to perform either sex role was known to be highly flexible depending on various, but often confounding, factors. For the pond snail, we report that young and small snails tend to mate as males first, though old and large snails do not seem to be better females.

Behavioural and physiological effects of population density on domesticated Zebra Finches (Taeniopygia guttata) held in aviaries

Zebra Finches (Taeniopygia guttata) are highly social and monogamous birds that display relatively low levels of aggression and coordinate group life mainly by means of vocal communication. In the wild, small groups may congregate to larger flocks of up to 150-350 birds. Little is known, however, about possible effects of population density on development in captivity. Investigating density effects on physiology and behaviour might be helpful in identifying optimal group size, in order to optimise Zebra Finch wellbeing. A direct effect of population density on development and reproduction was found: birds in lower density conditions produced significantly more and larger (body mass, tarsus length) surviving offspring than birds in high density conditions. Furthermore, offspring in low density aviaries produced slightly longer song motifs and more different syllables than their tutors, whereas offspring in high density aviaries produced shorter motifs and a smaller or similar number of different syllables than their tutors. Aggression levels within the populations were low throughout the experiment, but the number of aggressive interactions was significantly higher in high density aviaries. Baseline corticosterone levels did not differ significantly between high- and low density aviaries for either adult or offspring birds. On day 15 post hatching, brood size and baseline corticosterone levels were positively correlated. On days 60 and 100 post hatching this correlation was no longer present. The results of this study prove that population density affects various aspects of Zebra Finch development, with birds living in low population density conditions having an advantage over those living under higher population density conditions.

Non‐associative learning in the squid lolliguncula brevis (Mollusca, Cephalopoda)

Habituation and dishabituation are demonstrated for the first time in a squid (Cephalopoda: Teuthoidea). Each squid (n = 29) was exposed briefly to a plastic model of a predator to determine how the behavioural responses changed with repeated trials at 1 min intervals. Behavioural responses were video‐monitored for subsequent measurements of the number of escape jets and the duration of neurally controlled body pattern rings on each trial. Squids habituated readily to a teleost fish model and could differentiate clearly between a teleost fish and a shark model of the same size. Following a single series of 15 trials, habituated responses recovered after a 1 hr rest. Habituated responses also recovered rapidly (dishabituation) when a noxious stimulus was presented. Spaced Training was more effective than Massed Training in producing longer‐term habituation.

Maximized song learning of juvenile male zebra finches following BDNF expression in the HVC

During song learning, vocal patterns are matched to an auditory memory acquired from a tutor, a process involving sensorimotor feedback. Song sensorimotor learning and song production of birds is controlled by a set of interconnected brain nuclei, the song control system. In male zebra finches, the beginning of the sensorimotor phase of song learning parallels an increase of the brain‐derived neurotrophic factor (BDNF) in just one part of the song control system, the forebrain nucleus HVC. We report here that transient BDNF‐mRNA upregulation in the HVC results in a maximized copying of song syllables. Each treated bird shows motor learning to an extent similar to that of the selected best learners among untreated zebra finches. Because this result was not found following BDNF overexpression in the target areas of HVC within the song system, HVC‐anchored mechanisms are limiting sensorimotor vocal learning.