Social Interactions of Dat-Het Epi-Genotypes Differing for Maternal Origins: The Development of a New Preclinical Model of Socio-Sexual Apathy

Social interaction is essential for life but is impaired in many psychiatric disorders. We presently focus on rats with a truncated allele for dopamine transporter (DAT). Since heterozygous individuals possess only one non-mutant allele, epigenetic interactions may unmask latent genetic predispositions. Homogeneous “maternal” heterozygous offspring (termed MAT-HET) were born from dopamine-transporter knocked-out (DAT-KO) male rats and wild-type (WT) mothers; “mixed” heterozygous offspring (termed MIX-HET) were born from both DAT-heterozygous parents. Their social behavior was assessed by: partner-preference (PPT), social-preference (SPT) and elicited-preference (EPT) tests. During the PPT, focal MIX-HET and MAT-HET males had a choice between two WT females, one in estrous and the other not. In the SPT, they met as stimulus either a MIX-HET or a WT male. In the EPT, the preference of focal male WT rats towards either a MIX- or a MAT-HET stimulus was tested. MIX-HET focal males showed an abnormal behavior, seeming not interested in socializing either with a female in estrous or with another male if MIX-HET. Focal MAT-HET males, instead, were very attracted by the female in estrous, but totally ignored the MIX-HET male. We assessed the expression of noradrenaline transporter (NET) in prefrontal cortex, hippocampus and hypothalamus, finding differences between the two offspring. MIX-HETs’ hypothalamus and hippocampus showed less NET than MAT-HETs, while the latter, in turn, showed higher NET than WTs. These behavioral differences between heterozygous groups may be attributed to different maternal cares received. Results allow preclinical understanding of epigenetic factors involved in social-behavior abnormalities, typical of many psychiatric disorders.

Evidence of sperm removal behaviour in an externally fertilizing species and compensatory behaviour for the risk of self-sperm removal

The removal of rival sperm from a female's sperm storage organ acts as a strong sperm competition avoidance mechanism, which has been reported only in internally fertilizing species and not at all in externally fertilizing species. This study demonstrated for the first time that nest-holding males of Bathygobius fuscus , an externally fertilizing marine fish, remove the sperm of rival sneaker males from the spawning nest by exhibiting tail-fanning behaviour within the nest. Males showed tail-fanning behaviour when semen was artificially injected into the nest but not when seawater was injected, and in open nests this behaviour resulted in higher paternity rates for the focal male. The sperm removal behaviour entails the risk of removing their own sperm; therefore, additional sperm release behaviour is likely necessary to benefit from the sperm removal effect. Consistent with this, males increased post-fanning sperm release behaviour more in the semen than in the seawater injection treatment. Moreover, males who had removed sperm for a longer time spent more time releasing sperm after the removal, suggesting that the additional sperm release behaviour compensated for the loss of their own sperm. These results suggest that sperm removal behaviour is not restricted to internally fertilizing organisms and deserves further investigation in this and other species.

Testing predictions of inclusive fitness theory in inbreeding relatives with biparental care

Inclusive fitness theory predicts that parental care will vary with relatedness between potentially caring parents and offspring, potentially shaping mating system evolution. Systems with extra-pair paternity (EPP), and hence variable parent–brood relatedness, provide valuable opportunities to test this prediction. However, existing theoretical and empirical studies assume that a focal male is either an offspring's father with no inbreeding, or is completely unrelated. We highlight that this simple dichotomy does not hold given reproductive interactions among relatives, complicating the effect of EPP on parent–brood relatedness yet providing new opportunities to test inclusive fitness theory. Accordingly, we tested hierarchical hypotheses relating parental feeding rate to parent–brood relatedness, parent kinship and inbreeding, using song sparrows ( Melospiza melodia ) experiencing natural variation in relatedness. As predicted, male and female feeding rates increased with relatedness to a dependent brood, even controlling for brood size. Male feeding rate tended to decrease as paternity loss increased, and increased with increasing kinship and hence inbreeding between socially paired mates. We thereby demonstrate that variation in a key component of parental care concurs with subtle predictions from inclusive fitness theory. We additionally highlight that such effects can depend on the underlying social mating system, potentially generating status-specific costs of extra-pair reproduction.

Sperm allocation strategies in a sperm heteromorphic insect

Theories predict that in polyandrous species, the focal male should increase sperm allocation per mate in the presence of rivals to gain greater share of paternity, but in the presence of additional mates, he should reduce sperm allocation per mate to save sperm for insemination of more mates. However, empirical findings are often inconsistent and reasons behind are unclear. Furthermore, many studies use copulation duration as an estimate of the number of sperm transferred. Yet, empirical evidence for such assumption is largely lacking. Here, we used a sperm heteromorphic insect Ephestia kuehniella whose males produce two types of sperm, eupyrenes (fertile) and apyrenes (nonfertile), to test these postulations. We allowed focal males to detect chemical and acoustic but no tactile cues from rivals or additional mates both before and during mating and measured copulation duration and sperm allocation in successive copulations. We demonstrate that males transfer significantly more eupyrenes per mate in the presence of rivals and that the sperm allocation pattern persists in successive copulations under this condition. However, males do not adjust apyrene allocation in response to rivals probably because apyrenes play a relatively minor role in male reproductive success. Contrary to a previous study, focal males do not respond to additional mates most likely due to the lack of tactile cues in the present study. We reveal that sperm allocation is not a function of copulation duration in this insect for spermatophore formation and delivery occupy most of copulation duration and sperm transfer is complete near the end of copulation.

Gustatory cues to kinship among males moderate the productivity of females

Males of many species harm females as a byproduct of intrasexual competition, but this harm can be reduced if males are less competitive in the presence of familiar relatives. We determined the cue males use to identify competitors in this context. We assessed genetic variance in a putative kin recognition trait (cuticular hydrocarbons) in male seed beetles Callosobruchus maculatus and found that five hydrocarbons had significant components of additive genetic variance and could serve as relatedness cues. Next, we tested whether hydrocarbons were the mechanism males use to distinguish the social identities of competitors when strategically adjusting their competitiveness/harmfulness. Pairs of female and male C. maculatus were mated in the presence of hydrocarbons extracted from males that differed in their relatedness and familiarity to the focal male. Females were more productive after mating in the presence of extracts from the focal male’s nonrelatives, if those extracts were also unfamiliar to the focal male. Relatedness had no effect on productivity when extracts were familiar to the focal male. These results may be reconciled with those of previous studies that manipulated the relatedness and familiarity of competing males if the difference between the effect of harmfulness on productivity following a single mating and the effect on lifetime reproductive fitness after multiple matings is accounted for. This study provides a novel demonstration of the mechanism of social recognition in the moderation of sexual conflict.

Sex-specific responses to sexual familiarity, and the role of olfaction in Drosophila

Studies of mating preferences have largely neglected the potential effects of individuals encountering their previous mates (‘directly sexually familiar’), or new mates that share similarities to previous mates, e.g. from the same family and/or environment (‘phenotypically sexually familiar’). Here, we show that male and female Drosophila melanogaster respond to the direct and phenotypic sexual familiarity of potential mates in fundamentally different ways. We exposed a single focal male or female to two potential partners. In the first experiment, one potential partner was novel (not previously encountered) and one was directly familiar (their previous mate); in the second experiment, one potential partner was novel (unrelated, and from a different environment from the previous mate) and one was phenotypically familiar (from the same family and rearing environment as the previous mate). We found that males preferentially courted novel females over directly or phenotypically familiar females. By contrast, females displayed a weak preference for directly and phenotypically familiar males over novel males. Sex-specific responses to the familiarity of potential mates were significantly weaker or absent in Orco 1 mutants, which lack a co-receptor essential for olfaction, indicating a role for olfactory cues in mate choice over novelty. Collectively, our results show that direct and phenotypic sexual familiarity is detected through olfactory cues and play an important role in sex-specific sexual behaviour.

A comparison of two methods to assess audience-induced changes in male mate choice

Multidirectional communicative interactions in social networks can have a profound effect on mate choice behavior. Male Atlantic molly Poecilia mexicana exhibit weaker mating preferences when an audience male is presented. This could be a male strategy to reduce sperm competition risk: interacting more equally with different females may be advantageous because rivals might copy mate choice decisions. In line with this hypothesis, a previous study found males to show a strong audience effect when being observed while exercising mate choice, but not when the rival was presented only before the choice tests. Audience effects on mate choice decisions have been quantified in poeciliid fishes using association preference designs, but it remains unknown if patterns found from measuring association times translate into actual mating behavior. Thus, we created five audience treatments simulating different forms of perceived sperm competition risk and determined focal males’ mating preferences by scoring pre-mating (nipping) and mating behavior (gonopodial thrusting). Nipping did not reflect the pattern that was found when association preferences were measured, while a very similar pattern was uncovered in thrusting behavior. The strongest response was observed when the audience could eavesdrop on the focal male’s behavior. A reduction in the strength of focal males’ preferences was also seen after the rival male had an opportunity to mate with the focal male’s preferred mate. In comparison, the reduction of mating preferences in response to an audience was greater when measuring association times than actual mating behavior. While measuring direct sexual interactions between the focal male and both stimulus females not only the male’s motivational state is reflected but also females’ behavior such as avoidance of male sexual harassment.

A new member or an intruder: how do Sinai spiny mouse (Acomys dimidiatus) families respond to a male newcomer?

Recruitment of unrelated individuals into a group plays an important role in the social life of the group living animals. The main goal of our study was to analyze the reactions of established, breeding families of the Sinai spiny mouse, Acomys dimidiatus (Muridae, Rodentia), a social species with precocial pups, to male newcomers in the presence and the absence of a breeding resident male. We compared the behaviour of family members of different sex or age to the presence of a new male. The number of non-aggressive and aggressive interactions with the focal male (resident/newcomer male) was recorded during three periods: before, during and one month after the addition of the newcomer. Only a few aggressive and/or non-aggressive types of contacts occurred before and one month after the addition of the new male. During the experiment, both types of contacts arose, but the results were highly variable. Increased aggressive behaviour of the family toward the intruder was explained mainly by the presence of pregnant or lactating females, which suggests that aggression towards a male newcomer is associated with the reproductive status of females. This phenomenon is most likely connected with the counter-infanticide strategy.

Familiarity and threat of opponents determine variation in Thomas langur (Presbytis thomasi) male behaviour during between-group encounters

During between-group encounters in primates, males often defend mates, food or infants against other males. Males, however, show variation in contests between opponents. In other taxa, such variation has been attributed to variation in familiarity with or threat of opponents. Here we present the results of analyses of between-group encounter intensity variation in Thomas langurs while controlling for threat when evaluating familiarity and vice versa. Encounter intensity was measured by the proportion of encounters with chases and the number of loud calls per minute during the encounter given by the focal male. The results indicate that both familiarity and threat influence encounter intensity. Less familiar opponents had more intense encounters and opponents that differed in the threat level to each other also had more intense encounters. Thus, Thomas langur males seem to incorporate information on both the level of threat and familiarity of other males to make a decision on how to react during a between-group encounter.

Singing Complexity of The Banded Wren (Thryothorus Pleurostictus): Do Switching Rate and Song-Type Diversity Send Different Messages?

Most species of songbird possess repertoires of song types or variations that allow singers to vary how they present their songs. “Complexity,” or the amount of variation in a singing performance, has several distinct components that include the number of song types used, variation within song types, and rate of switching between song types. Because singers can control each factor somewhat independently, different components may encode different kinds of information. In a series of interactive playbacks, I presented Banded Wrens (Thryothorus pleurostictus) with stimuli that altered song-type diversity and switching rates independently. My results show that switching rates affect males' aggressive approach responses, with lower switching rates eliciting stronger responses. By contrast, song-type diversity does not appear to affect males' approach responses when switching rates are held at a high and constant level. Although focal male switching rates and song-type diversity are not strongly influenced by playback type, males frequently respond to high-diversity playback with delayed matches. Delayed matching entails using one or more of the same song types from the playback, without immediate song- type matching. Although delayed matches occurred at levels above chance during high-diversity playbacks, focal males appeared to avoid them during other types of playback; immediate matches were rare and repertoire matches frequent for all playback treatments. Overall, males' responses to the three playback stimuli suggest that switching rate and song-type diversity encode different messages.Complejidad del Canto de Thryothorus pleurostictus: ¿Envían Diferentes Mensajes las Tasas de Cambio y la Diversidad de Tipos de Canto?