Conserved transcriptomic profiles underpin monogamy across vertebrates.
ABSTRACT: Social monogamy, typically characterized by the formation of a pair bond, increased territorial defense, and often biparental care, has independently evolved multiple times in animals. Despite the independent evolutionary origins of monogamous mating systems, several homologous brain regions and neuropeptides and their receptors have been shown to play a conserved role in regulating social affiliation and parental care, but little is known about the neuromolecular mechanisms underlying monogamy on a genomic scale. Here, we compare neural transcriptomes of reproductive males in monogamous and nonmonogamous species pairs of Peromyscus mice, Microtus voles, parid songbirds, dendrobatid frogs, and Xenotilapia species of cichlid fishes. We find that, while evolutionary divergence time between species or clades did not explain gene expression similarity, characteristics of the mating system correlated with neural gene expression patterns, and neural gene expression varied concordantly across vertebrates when species transition to monogamy. Our study provides evidence of a universal transcriptomic mechanism underlying the evolution of monogamy in vertebrates.
Project description:We compare fore- and mid-brain transcriptomes of reproductive males in monogamous and non-monogamous species pairs of Peromyscus mice, Microtus voles, parid songbirds, dendrobatid frogs, and Xenotilapia species of cichlid fishes. Our study provides evidence of a universal transcriptomic mechanism underlying the evolution of monogamy in vertebrates. Overall design: Fore- and mid-brain mRNA of reproductive males samples (n=3) were pooled and sequenced using an Illuma HiSeq platform.
Project description:Throughout the animal kingdom, we know many examples of mating system evolution that exemplify adaptive responses to changes in the environment, yet our understanding of the accompanying neural and molecular mechanisms that give rise to such behavioral changes remains understudied. In the present study we aimed to define the molecular basis of interspecific variation in social organization in Ectodini cichlids from Lake Tanganyika. We selected four closely related species that represent two independent evolutions of monogamy: the polygynous Xenotilapia ochrogenys, the monogamous Xenotilapia flavipinnis, the polygynous Microdontochromis tenuidentata and the monogamous Asprotilapia leptura. Using a single cichlid microarray platform, we conducted a total of 28 direct comparisons for neural gene expression level among males and 26 among females of four species that represent 2 independent evolutions of monogamy. Our results indicate the gene expression profiles display remarkable plasticity across different time scales because we find differences associated with sex, mating system, and lineage. Overall design: We used a nested loop design with dye-swap to emphasize within-lineage comparison between species of different mating strategies. This data series represents males and females only and includes, for each sex, 9 arrays comparing inidividuals from 2 differeent species with different mating types (monogomous and polygamous)within the xenotilaipa lineage and 9 arrays comparing individuals from two different species of different mating types (polygamovus vs. monogomous) in the non-xenotilapia-lineage. There are 8 hybridizations that compare between the two lineages 4 of which are within-mating strategy and 4 of which are between mating strategy. Features have been filtered for sequence conservation across species under study.
Project description:Classic evolutionary theory predicts that monogamy should be intimately linked with parental care. It has long been assumed, therefore, that avian brood parasites-which lay their eggs in the nests of 'host' species and provide little, if any, parental care-should be overwhelmingly promiscuous. However, recent studies have revealed that the social mating systems of brood parasites are surprisingly diverse, encompassing lek polygyny, monogamy, polygamy and promiscuity. What ecological or phylogenetic factors explain this variation, and why are some brood parasites apparently monogamous? Here we review the social and genetic mating systems of all 75 brood parasitic species for which data are available and evaluate several hypotheses that may help explain these patterns. We find that social monogamy is widespread, often co-occurring with territoriality and cooperative behaviour by the mated pair. Comparative studies, though preliminary, suggest that in some species, monogamy is associated with low host density and polygamy with higher host density. Interestingly, molecular data show that genetic and social mating systems can be entirely decoupled: genetic monogamy can occur in parasitic species that lack behavioural pair-bonds, possibly as a by-product of territoriality; conversely, social monogamy has been reported in parasites that are genetically polygamous. This synthesis suggests that social and genetic monogamy may result from very different selective pressures, and that male-female cooperative behaviours, population density and territoriality may all interact to favour the evolution of monogamous mating in brood parasites. Given that detailed descriptive data of social, and especially genetic, mating systems are still lacking for the majority of brood parasitic species, definitive tests of these hypotheses await future work. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.
Project description:Despite its well-described role in female affiliation, the influence of oxytocin on male pairbonding is largely unknown. However, recent human studies indicate that this nonapeptide has a potent influence on male behaviors commonly associated with monogamy. Here we investigated the distribution of oxytocin receptors (OTR) throughout the forebrain of the socially monogamous male prairie vole (Microtus ochrogaster). Because males vary in both sexual and spatial fidelity, we explored the extent to which OTR predicted monogamous or non-monogamous patterns of space use, mating success and sexual fidelity in free-living males. We found that monogamous males expressed higher OTR density in the nucleus accumbens than non-monogamous males, a result that mirrors species differences in voles with different mating systems. OTR density in the posterior portion of the insula predicted mating success. Finally, OTR in the hippocampus and septohippocampal nucleus, which are nuclei associated with spatial memory, predicted patterns of space use and reproductive success within mating tactics. Our data highlight the importance of oxytocin receptor in neural structures associated with pairbonding and socio-spatial memory in male mating tactics. The role of memory in mating systems is often neglected, despite the fact that mating tactics impose an inherently spatial challenge for animals. Identifying mechanisms responsible for relating information about the social world with mechanisms mediating pairbonding and mating tactics is crucial to fully appreciate the suite of factors driving mating systems. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.
Project description:Complex social behavior in Microtus voles and other mammals has been postulated to be under the direct genetic control of a single locus: the arginine vasopressin 1a receptor (avpr1a) gene. Using a phylogenetic approach, we show that a repetitive element in the promoter region of avpr1a, which reportedly causes social monogamy, is actually widespread in nonmonogamous Microtus and other rodents. There was no evidence for intraspecific polymorphism in regard to the presence or absence of the repetitive element. Among 25 rodent species studied, the element was absent in only two closely related nonmonogamous species, indicating that this absence is certainly the result of an evolutionarily recent loss. Our analyses further demonstrate that the repetitive structures upstream of the avpr1a gene in humans and primates, which have been associated with social bonding, are evolutionarily distinct from those in rodents. Our evolutionary approach reveals that monogamy in rodents is not controlled by a single polymorphism in the promoter region of the avpr1a gene. We thus resolve the contradiction between the claims for an evolutionarily conserved genetic programming of social behavior in mammals and the vast evidence for highly complex and flexible mating systems.
Project description:Animals with socially monogamous mating systems are valuable for discovering proximate mechanisms of prosocial behavior and close social relationships. Especially powerful are comparisons between related species that differ in monogamous tendency. Birds are the most socially monogamous vertebrates. Thus far most research on mechanisms of pairing has used zebra finches, which do not have a relative with a different mating system, however. The goal of the experiments reported here was to develop a new comparative avian system by studying the pairing behavior of a reportedly strongly monogamous quail, the king quail (Coturnix chinensis), a species in the same clade as the less monogamous Japanese quail (Coturnix japonica), the subject of much prior research. In Experiment 1 male-female pairs of king quail housed together were initially avoidant or aggressive but most rapidly progressed to allopreening and huddling. A separation-reunion paradigm reliably elicited both of these behaviors in males that had cohabited for one week. In Experiment 2 the allopreening and huddling behavior of males in cohabiting pairs was highly selective, and a majority of the males were aggressive toward a familiar female that was not the cohabitation partner. In Experiment 3 males were separated from their female cohabitation partners for 9-10 weeks and then given two-choice tests. All but one male spent more time near an unfamiliar female, which may have reflected aggression and shows recognition of and memory for the past pairing experience. Thus king quail show robust, selective and easy to measure pairing behavior that can be reliably elicited with simple separation-reunion testing procedures. Copulation is rarely seen during tests. The behavior of king quail is a striking contrast to that of Japanese quail, providing a new comparative system for discovering mechanisms of behavior related to close social relationships and monogamy.
Project description:Polyandrous mating is common, but the benefits for females of polyandry remain controversial. To test whether mating with multiple males affects female fitness, we compared lifetime components of fitness of three experimental sets of Drosophila pseudoobscura females: monogamous females allowed to copulate one time (MOC); monogamous females held with a male over her entire life and experiencing many copulations (MMC); and polyandrous females with a different male over each day of their lives and also experiencing many copulations (PMC). Consistent with previous studies in this species, females in treatments in which multiple copulations occurred, MMC and PMC, had offspring with significantly higher egg-to-adult survival (i.e., offspring viability) and higher numbers of adult offspring (i.e., productivity) than MOC females, showing that multiple inseminations enhance offspring and mother fitness. In addition, although MMC females laid significantly more eggs than polyandrous (PMC) females, percent egg-to-adult survival and number of adult offspring were higher for PMC than MMC females, showing that polyandrous mating enhances the fitness of females more than multiply mating with only one male. Inconsistent with the cost of reproduction, lifespan was not significantly longer for MOC females than for MMC or PMC females. To our knowledge, this is the first study to examine simultaneously in outbred WT Drosophila pseudoobscura the lifetime costs and benefits to females of polyandry, monogamy with a single copulation, and monogamy with repeat copulations.
Project description:Non-monogamous mating behaviors including polygyny or extra-pair paternity are theorized to amplify sexual selection, since some males attract multiple mates or copulate with paired females. In several well-studied songbird species, females prefer more complex songs and larger repertoires; thus, non-monogamous mating behaviors are predicted to accelerate song evolution, particularly toward increased complexity. However, studies within songbird clades have yielded mixed results, and the effect of non-monogamy on song evolution remains unclear. Here, we construct a large-scale database synthesizing mating system, extra-pair paternity, and song information and perform comparative analyses alongside songbird genetic phylogenies. Our results suggest that polygyny drives faster evolution of syllable repertoire size (measured as average number of unique syllables), but this rapid evolution does not produce larger repertoires in polygynous species. Instead, both large and small syllable repertoires quickly evolve toward moderate sizes in polygynous lineages. Contrary to expectation, high rates of extra-pair paternity coincide with smaller repertoires.
Project description:Larger testes produce more sperm and therefore improve reproductive success in the face of sperm competition. Adaptation to social mating systems with relatively high and low sperm competition are therefore likely to have driven changes in relative testes size in opposing directions. Here, we combine the largest vertebrate testes mass dataset ever collected with phylogenetic approaches for measuring rates of morphological evolution to provide the first quantitative evidence for how relative testes mass has changed over time. We detect explosive radiations of testes mass diversity distributed throughout the vertebrate tree of life: bursts of rapid change have been frequent during vertebrate evolutionary history. In socially monogamous birds, there have been repeated rapid reductions in relative testes mass. We see no such pattern in other monogamous vertebrates; the prevalence of monogamy in birds may have increased opportunities for investment in alternative behaviours and physiologies allowing reduced investment in expensive testes.
Project description:BACKGROUND: Phylogenetic analyses strongly associate nonsocial ancestors of cooperatively-breeding or eusocial species with monogamy. Because monogamy creates high-relatedness family groups, kin selection has been concluded to drive the evolution of cooperative breeding (i.e., the monogamy hypothesis). Although kin selection is criticized as inappropriate for modeling and predicting the evolution of cooperation, there are no examples where specific inclusive fitness-based predictions are intrinsically wrong. The monogamy hypothesis may be the first case of such a flawed calculation. RESULTS: A simulation model mutated helping alleles into non-cooperative populations where females mated either once or multiply. Although multiple mating produces sibling broods of lower relatedness, it also increases the likelihood that one offspring will adopt a helper role. Examining this tradeoff showed that under a wide range of conditions polygamy, rather than monogamy, allowed helping to spread more rapidly through populations. Further simulations with mating strategies as heritable traits confirmed that multiple-mating is selectively advantageous. Although cooperation evolves similarly regardless of whether dependent young are close or more distant kin, it does not evolve if they are unrelated. CONCLUSIONS: The solitary ancestral species to cooperative breeders may have been predominantly monogamous, but it cannot be concluded that monogamy is a predisposing state for the evolution of helping behavior. Monogamy may simply be coincidental to other more important life history characteristics such as nest defense or sequential provisioning of offspring. The differing predictive outcome from a gene-based model also supports arguments that inclusive fitness formulations poorly model some evolutionary questions. Nevertheless, cooperation only evolves when benefits are provided for kin: helping alleles did not increase in frequency in the absence of potential gains in indirect fitness. The key question, therefore, is not whether kin selection occurs, but how best to elucidate the differing evolutionary advantages of genetic relatedness versus genetic diversity.