Genetic monogamy despite social promiscuity in the pot-bellied seahorse (Hippocampus abdominalis)

Sexual selection theory predicts a positive correlation between relative parental investment and mate choice. In syngnathid fishes (seahorses and pipefish), males brood offspring in specialized brooding structures. While female-female mating competition has been demonstrated in some pipefishes, all seahorses (genus Hippocampus) studied to date have been found to have conventional sex roles with greater male-male competition for access to mates despite possessing the most complex brood structures in the family. Although multiple mating is common in pipefish, seahorses are again exceptional, exhibiting strict genetic monogamy. Both demographic and behavioural explanations have been offered to explain the lack of multiple mating in seahorse species, but these hypotheses have not yet been explicitly addressed. We investigated mating systems and brood parentage of the pot-bellied seahorse, Hippocampus abdominalis, a temperate-water species that is socially promiscuous with conventional sex roles in laboratory populations. We observed promiscuous courtship behaviour and sex-role reversal in high density, female-biased field populations of H. abdominalis. We hypothesize that sex roles are plastic in H. abdominalis, depending on local population density and sex ratio. Despite promiscuous courtship behaviour, all assayed male seahorses were genetically monogamous in both laboratory and wild populations. Physiological limitations associated with embryo incubation may explain the absence of multiple mating in seahorses and may have played an important role in the development of the unique reproductive behaviour typical in these species.     

Microsatellite evidence for monogamy and sex-biased recombination in the Western Australian seahorse Hippocampus angustus

Four polymorphic microsatellite loci were used to assess biological parentage of 453 offspring from 15 pregnant males from a natural population of the Western Australian seahorse Hippocampus angustus . Microsatellite genotypes in the progeny arrays were consistent with a monogamous mating system in which both females and males had a single mate during a male brooding period. Multilocus genotypes implicated four females in the adult population sample as contributors of eggs to the broods of collected males, but there was no evidence for multiple mating by females. Based on genotypic data from the progeny arrays, two loci were linked tightly and the recombination rate appeared to be ≈ 10-fold higher in females than in males. The utility of linked loci for parentage analyses is discussed.     

Population dynamics of the long-snouted seahorse (Hippocampus guttulatus Cuvier, 1829) in the Mar Menor coastal lagoon

A 10-year monitoring program was developed to quantify the population dynamics of the long-snouted seahorse population in the Mar Menor coastal lagoon. Based on 985 underwater visual censuses, we estimated the long-snouted seahorse (Hippocampus guttulatus Cuvier, 1829) population size in the Mar Menor lagoon and its reduction in size in the last decades, as well as the effect of eutrophication crises in 2016 and 2019 on the species. The annual recruitment for the 2013–2020 period was estimated by comparing the relative abundance of early seahorse life stages in the ichthyoplankton. The density ranged from 0.0458 specimens/m³ at the beginning of the sampling period to 0.0004 at the end, showing a statistically significant difference between the three analyzed periods (H_gl=2 = 14.0, p = 0.001). The long-snouted seahorse population from the Mar Menor lagoon exemplifies the impact of fishing activities and human pressure, especially euxinic episodes and habitat destruction. As a result of this, the Mar Menor population has decreased from several million specimens to a few thousand, in only three decades. This species showed considerable resilience, the seahorse population began to recover once fishing activity stopped. In contrast, the long-snouted seahorse showed high vulnerability to habitat loss and an episodic flooding event. Adult seahorses showed preferences for highly complex habitats, especially Caulerpa prolifera–Cymodocea nodosa mixed meadows and habitats of high complexity and anthropogenic origin, such as harbors, jetties, or breakwaters. In contrast, juvenile seahorses preferred monotonous seabeds with low complexity, such as the sandy beds that are characteristic of the Mar Menor lagoon littoral.     

Serial monogamy and sex ratio bias in Nazca boobies

Biased operational sex ratios (OSRs) can drive sexual selection on members of the over-represented sex via competition for mates, causing higher variance and skew in reproductive success (RS) among them if an individual's quality is a persistent characteristic. Alternatively, costs of reproduction may degrade breeding performance, creating the opportunity for members of the limiting sex to switch mates adaptively, effectively homogenizing variance and skew in RS among the sex in excess. We tested these two contrasting models in a male-biased population of the Nazca booby (Sula granti) with demonstrated costs of reproduction with data on total RS over a 14-year period. Variances and skews in RS were similar, and males changed from breeder to non-breeder more frequently than females. Under the persistent individual quality model, females should mate only with high quality males, and non-breeding males should seldom enter the breeding pool, yet 45% of non-breeding males (re)entered the breeding pool each year on average. Many Nazca booby females apparently exchange a depleted male for a new mate from the pool of current non-breeder males. Our evidence linking serial monogamy to costs of reproduction is novel and suggests selection on female mating preferences based on an interaction between at least two life-history components (OSR and reproductive effort).     

Genetic monogamy in the Common Crossbill ( Loxia curvirostra )

Extrapair paternity seems to be common in socially monogamous passerines, but the genetic mating system of most species is currently unknown. Here, we report the first study of paternity in the socially monogamous Common Crossbill (Loxia curvirostra). We found no evidence of extrapair paternity among 96 offspring in 34 examined broods. An upper 95% confidence limit of 3.1% suggests that extrapair fertilizations were truly infrequent in our study population. Common Crossbills thus seem to represent an exception to the rule of extrapair mating among socially monogamous passerine bird species. A potentially important selective pressure preventing promiscuity in Common Crossbills is the harsh environmental conditions experienced during breeding at wintertime, which may increase the importance of paternal care and limit the time available for seeking extrapair copulations.     

Mate choice, operational sex ratio, and social promiscuity in a wild population of the long-snouted seahorse Hippocampus guttulatus

Mate competition and mate choice are not mutually exclusivebehaviors. Both behaviors may drive sexual selection in oneor both sexes of a population. One of several factors affectingwhich behavior is exhibited by which sex is the operationalsex ratio (OSR) in the study population. The present study combinesbehavioral observations in the field with controlled experimentsin aquaria to investigate social interactions and mate choicein both male and female long-snouted seahorses Hippocampus guttulatusin the context of the population OSR. Compared with the morereadily studied pipefishes, data on OSR and mate choice in seahorsesare scarce in the published literature. Our field data providenovel evidence of social promiscuity, size-assortative mating,and an OSR that varies from being unbiased early and midseasonto male biased at the end of the breeding season. Our mate choiceexperiments revealed intersexual differences in mate preferencewith males significantly preferring larger females to familiarones. Taken together, our field and experimental results suggestthat mate choice rather than intrasexual competition could drivesexual selection in seahorses.     

Novel microsatellite loci in the threatened European long-snouted seahorse (<Emphasis Type="Italic">Hippocampus guttulatus</Emphasis>) for genetic diversity and parentage analysis

The long-snouted seahorse Hippocampus guttulatus is one of the two European seahorse species. We describe the isolation of the first 12 microsatellite loci in this threatened species. These new markers were tested in non-invasive samples of 32 seahorses from NW Spain. The number of alleles ranged from 2 to 15 (mean: 6.3) and expected heterozygosity from 0.031 to 0.912 (mean: 0.500). All loci conformed to Hardy–Weinberg expectations and no genotypic disequilibrium was observed between any pair of loci. The theoretical exclusion probabilities for this set of loci, when no parental information exists or when one parent is known, were 0.973 and 0.998, respectively. This study indicates the usefulness of these novel loci for population analysis and kinship studies in Hippocampus guttulatus. Their potential application is extended to the other European seahorse species, since all loci were successfully cross-amplified in H. hippocampus.     

A sedentary fish on the move: effects of displacement on long-snouted seahorse (Hippocampus guttulatus Cuvier) movement and habitat use

To understand how a sedentary fish responds to displacement and identify key habitat characteristics for that fish, we translocated long-snouted seahorses (Hippocampus guttulatus) within their natural habitat but far beyond their home range. After displacement, we located these small fish using acoustic technology and collected environmental data where we captured, released, and relocated them. Displaced fish (n?=?9) moved much greater distances (max: 150?m; mean daily: 6.4?C48.2?m) than expected from known home range movements and there was no evidence of homing. Seahorses varied in the specific environments they moved towards but tended to move towards environments more similar in both depth and water current speed to their original capture locations than their release locations.     

Female aggression and the maintenance of monogamy: female behaviour predicts male mating status in European starlings

Any reduction in the fitness of a breeding female induced by the settlement of additional females with her mate creates a conflict between the sexes over mating system. In birds, females are often aggressive towards other females but few studies have been able to quantify the importance of female-female aggression for the maintenance of monogamy. This study of the European starling, Sturnus vulgaris, quantifies male and female behaviour towards a potential prospecting female, presented in a cage during the pre-laying period, and relates it to the subsequent mating status of the male. A solitary breeding male was given the opportunity to attract an additional mate, which almost half of the males did. No biometric characters of the male or female were related to the subsequent mating status. Males demonstrated mate-attraction behaviour towards the caged female but the behaviour of the male did not predict the likelihood to attract an additional female. However, the proportion of time that the female spent near the potential settler was related to mating status, indicating that females that reacted more strongly towards a potential female competitor maintained their monogamous status. These results suggest that female behaviour may play an important role in shaping the mating system of facultatively polygynous species.     

Life history and ecology of the elusive European short‐snouted seahorse Hippocampus hippocampus

To improve the understanding of the life history and ecology of one of Europe's most elusive fishes, the short‐snouted seahorse Hippocampus hippocampus, data from wild populations in a shallow coastal lagoon in southern Portugal were analysed. The data were collected from 17 tagged seahorses on a focal‐study grid as well as from >350 seahorses encountered during underwater visual surveys and a fishery‐independent study using beach seines. These populations of settled juveniles and adults had a mean population density of 0·009 m^?2. During the study period (2000–2004), reproduction peaked in July and August. Juveniles recruited to the lagoon at c. 66 mm standard length (L_S) and 0·5 years of age and established small home ranges (0·8 to 18·2 m²). First reproduction was estimated at 100 mm and 1 year of age. Based on a fitted von Bertalanffy model, H. hippocampus grew quickly (growth coefficient K = 0·93) to a maximum theoretical size L_∞ = 150 mm and have a maximum lifespan of c. 3·2 years. Courtship behaviours were consistent with the maintenance of pair bonds and males brooded multiple batches of young per year. Estimated annual reproductive output averaged 871 young (±632). Together these analyses provide the first life‐history parameters for this species and indicate that H. hippocampus bears characteristics of opportunist and intermediate strategists. Such populations are predicted to exhibit large fluctuations in abundance, making them vulnerable to extended periods of poor recruitment.     

Genetic monogamy in Monteiro's hornbill, Tockus monteiri

Hornbills display a unique breeding habit in which the female seals herself into the nest cavity prior to egg laying and remains ensconced for most of the breeding cycle. This habit necessitates long-term sperm storage, which considerably lengthens the fertile period of the female. This in turn increases the amount of time available to females to engage in extrapair copulations. Because food delivered by the male is the primary source of energy for female maintenance, egg production, incubation, female moult and offspring provisioning, male parental investment (and thus cuckoldry) in these hornbills is extremely expensive. This combination of costly male parental care and female dependence potentially places hornbills at a critical endpoint in the spectrum of genetic promiscuity operating within pairs of socially monogamous birds. A paradigm of reproductive conflict suggests that these factors might allow males to coerce females into a state of genetic monogamy. Sperm storage, however, might allow female hornbills to thwart monopolization attempts by their mates. We used minisatellite multilocus DNA fingerprinting to analyse paternity in a Namibian population of Monteiro's hornbill, Tockus monteiri. Despite the ability of female hornbills to store sperm for long periods, we found no evidence of extrapair paternity (EPP). Although we cannot explicitly rule out a role for coercion in the evolution of the genetic monogamy we observed, the benefits of EPP appear to be devalued to the point that the reproductive interests of males and females overlap considerably. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Eight microsatellite loci characterised in the European blackbird, Turdus merula

Although the European blackbird, Turdus merula, is one of the most abundant and conspicuous songbirds of the Western Palaearctic and, as such, has been subject of numerous behavioural and ecological studies, there is to date no specific, PCR-based marker system for this species, and information on the applicability of genetic markers from other species or genera is scant. Here, we report the successful amplification of eight microsatellite loci in the European blackbird. We compared levels of polymorphism between groups of individuals sampled during the breeding season at different geographic localities (Heligoland Island, North Sea and Radolfzell, south-western Germany). We found high levels of polymorphisms, which enabled us to ascertain population membership of individuals. The properties of the tested microsatellite markers make them suitable for population genetic studies as well as for kinship analyses.     

Sexual dimorphism of egg size in the European Blackbird Turdus merula

Recently, a number of studies have shown that female birds are able to control the sex of their progeny at the stage of the gamete. There is also some evidence that females adjust their investment in offspring depending on the sex of the embryo during egg formation. Differential maternal investment to the eggs depending on their sex is usually interpreted as an adaptive strategy, by which females can increase competitive abilities of the smaller sex, or preferentially invest towards the sex with the potentially higher fitness returns. Here, we studied variation in egg size in relation to embryo sex and laying order in the European Blackbird Turdus merula. We found male and female eggs to differ in size, with larger eggs containing male embryos, as well as a significant interaction between embryo sex and laying order. This interaction resulted from the fact that egg size increased with the laying sequence among eggs bearing females but did not change with laying order among eggs bearing males. There was no relationship between offspring sex and the laying sequence within a clutch. We suggest that sexual dimorphism in egg size recorded in the European Blackbird may reflect favouritism of the sex which may give higher fitness returns.     

Historical and contemporary population genetic connectivity of the European short-snouted seahorse Hippocampus hippocampus and implications for management

This first genetic study of Hippocampus hippocampus covers the species' entire geographic range and employs two mtDNA markers (control region and cytochrome b) to establish patterns of population structuring. A total of 255 specimens from 21 locations were used to obtain 89 concatenated haplotypes. The common haplotype was present in all but one population, however, most haplotypes were unique. The haplotype network had a star-like construction, suggesting expansion from a bottleneck event. F(ST) and AMOVA revealed population subdivision into three geographic regions (English Channel + Bay of Biscay, Mediterranean Sea + Atlantic Ocean Iberian coast + Macaronesian Islands, and West Africa) with barriers to gene flow indentified at Cape Finisterre and the Cape Verde frontal zone. Neutrality tests and nested clade analysis suggest a complex demographic history, with both historic events and contemporary processes shaping patterns of genetic differentiation. The genetic population subdivision detected in this study indicates that H. hippocampus should be managed as three separate units. This is especially pertinent as H. hippocampus populations within the West African region are the only ones known to be specifically targeted for exploitation.