Brain size evolution in pipefishes and seahorses: the role of feeding ecology,life history and sexual selection

Brain size varies greatly at all taxonomic levels. Feeding ecology, life history and sexual selection have been proposed as key components in generating contemporary diversity in brain size across vertebrates. Analyses of brain size evolution have, however, been limited to lineages where males predominantly compete for mating and females choose mates. Here, we present the first original data set of brain sizes in pipefishes and seahorses (Syngnathidae) a group in which intense female mating competition occurs in many species. After controlling for the effect of shared ancestry and overall body size, brain size was positively correlated with relative snout length. Moreover, we found that females, on average, had 4.3% heavier brains than males and that polyandrous species demonstrated more pronounced (11.7%) female‐biased brain size dimorphism. Our results suggest that adaptations for feeding on mobile prey items and sexual selection in females are important factors in brain size evolution of pipefishes and seahorses. Most importantly, our study supports the idea that sexual selection plays a major role in brain size evolution, regardless of on which sex sexual selection acts stronger.     

The evolutionary origins of Syngnathidae: pipefishes and seahorses

Despite their importance as evolutionary and ecological model systems, the phylogenetic relationships among gasterosteiforms remain poorly understood, complicating efforts to understand the evolutionary origins of the exceptional morphological and behavioural diversity of this group. The present review summarizes current knowledge on the origin and evolution of syngnathids, a gasterosteiform family with a highly developed form of male parental care, combining inferences based on morphological and molecular data with paleontological evidence documenting the evolutionary history of the group. Molecular methods have provided new tools for the study of syngnathid relationships and have played an important role in recent conservation efforts. Despite recent insights into syngnathid evolution, however, a survey of the literature reveals a strong taxonomic bias towards studies on the species-rich genera Hippocampus and Syngnathus, with a lack of data for many morphologically unique members of the family. The study of the evolutionary pressures responsible for generating the high diversity of syngnathids would benefit from a wider perspective, providing a comparative framework in which to investigate the evolution of the genetic, morphological and behavioural traits of the group as a whole.     

Exploring gene-culture interactions: insights from handedness, sexual selection and niche-construction case studies

Genes and culture represent two streams of inheritance that for millions of years have flowed down the generations and interacted. Genetic propensities, expressed throughout development, influence what cultural organisms learn. Culturally transmitted information, expressed in behaviour and artefacts, spreads through populations, modifying selection acting back on populations. Drawing on three case studies, I will illustrate how this gene-culture coevolution has played a critical role in human evolution. These studies explore (i) the evolution of handedness, (ii) sexual selection with a culturally transmitted mating preference, and (iii) cultural niche construction and human evolution. These analyses shed light on how genes and culture shape each other, and on the significance of feedback mechanisms between biological and cultural processes.     

Adaptations to sexual selection and sexual conflict: insights from experimental evolution and artificial selection

Artificial selection and experimental evolution document natural selection under controlled conditions. Collectively, these techniques are continuing to provide fresh and important insights into the genetic basis of evolutionary change, and are now being employed to investigate mating behaviour. Here, we focus on how selection techniques can reveal the genetic basis of post-mating adaptations to sexual selection and sexual conflict. Alteration of the operational sex ratio of adult Drosophila over just a few tens of generations can lead to altered ejaculate allocation patterns and the evolution of resistance in females to the costly effects of elevated mating rates. We provide new data to show how male responses to the presence of rivals can evolve. For several traits, the way in which males responded to rivals was opposite in lines selected for male-biased, as opposed to female-biased, adult sex ratio. This shows that the manipulation of the relative intensity of intra- and inter-sexual selection can lead to replicable and repeatable effects on mating systems, and reveals the potential for significant contemporary evolutionary change. Such studies, with important safeguards, have potential utility for understanding sexual selection and sexual conflict across many taxa. We discuss how artificial selection studies combined with genomics will continue to deepen our knowledge of the evolutionary principles first laid down by Darwin 150 years ago.     

Mating games: cultural evolution and sexual selection

In this paper, we argue that mating games, a concept that denotes cultural practices characterized by a competitive element and an ornamental character, are essential drivers behind the emergence and maintenance of human cultural practices. In order to substantiate this claim, we sketch out the essential role of the game’s players and audience, as well as the ways in which games can mature and turn into relatively stable cultural practices. After outlining the life phase of mating games – their emergence, rise, maturation, and possible eventual decline – we go on to argue that participation in these games (in each phase) does make sense from an adaptationist point of view. The strong version of our theory which proposes that all cultural practices are, or once were, mating games, allows us to derive a set of testable predictions for the fields of archaeology, economics, and psychology.     

Male pregnancy and the evolution of body segmentation in seahorses and pipefishes

The evolution of complex traits, which are specified by the interplay of multiple genetic loci and environmental effects, is a topic of central importance in evolutionary biology. Here, we show that body and tail vertebral numbers in fishes of the pipefish and seahorse family (Syngnathidae) can serve as a model for studies of quantitative trait evolution. A quantitative genetic analysis of body and tail vertebrae from field-collected families of the Gulf pipefish, Syngnathus scovelli, shows that both traits exhibit significantly positive additive genetic variance, with heritabilities of 0.75 +/- 0.13 (mean +/- standard error) and 0.46 +/- 0.18, respectively. We do not find any evidence for either phenotypic or genetic correlations between the two traits. Pipefish are characterized by male pregnancy, and phylogenetic consideration of body proportions suggests that the position of eggs on the pregnant male's body may have contributed to the evolution of vertebral counts. In terms of numbers of vertebrae, tail-brooding males have longer tails for a given trunk size than do trunk-brooding males. Overall, these results suggest that vertebral counts in pipefish are heritable traits, capable of a response to selection, and they may have experienced an interesting history of selection due to the phenomenon of male pregnancy. Given that these traits vary among populations within species as well as among species, they appear to provide an excellent model for further research on complex trait evolution. Body segmentation may thus afford excellent opportunities for comparative study of homologous complex traits among disparate vertebrate taxa.     

The genetics and genomics of Syngnathidae: pipefishes, seahorses and seadragons

The goal of this review was to provide a historical overview of how molecular techniques have increased the understanding of the ecology and evolution of the family Syngnathidae (pipefishes, seahorses and seadragons). Molecular studies based primarily on mitochondrial DNA markers have proved their worth by elucidating complex phylogenetic relationships within the family. Phylogeographic studies, which have revealed how life-history traits and past climatic events shape geographic distributions and patterns of genetic variation within syngnathid species, also provide interesting case studies for the conservation and management of threatened species. The application of microsatellite DNA markers has opened a floodgate of studies concerned with the breeding biology of these fishes, which are interesting due to their unique reproductive mode of male pregnancy. Research in this area has contributed significantly to the understanding of mating patterns and sexual selection. Molecular markers may also be employed in studies of demography, migration and local breeding population sizes. Genomic studies have identified genes that are probably involved in male pregnancy and promise additional insights into various aspects of syngnathid biology at the level of the gene. Despite these advances, much more remains to be explored. Goals for future research should include: (1) a more inclusive phylogeny to resolve outstanding issues concerning the relationships within the family and higher order taxa, (2) a broader use of molecular studies to aid management and conservation efforts, (3) the inclusion of more genera in comparative behavioural studies and (4) the continued development of genomic resources for syngnathids to facilitate comparative genomic work.     

The importance of seahorses and pipefishes in the diet of marine animals

A review of 135 accounts of predation on seahorses and pipefishes identified 82 predator species, with nine species of seahorses and 25 of pipefishes recorded as prey. These cryptic fishes were generally depredated in low numbers. Where syngnathids formed a high proportion of predator diets, predation occurred on (1) a single abundant species during a population boom or large die-off, (2) concentrations of individuals utilising floating marine vegetation, or (3) juveniles when abundant during the breeding season. Predation coinciding with high syngnathid densities suggests their predators are foraging opportunistically rather than targeting syngnathids as prey. Invertebrates, fishes, sea turtles, waterbirds and marine mammals were all syngnathid predators: these included taxa that do not frequent the demersal habitat generally occupied by seahorses and pipefishes. Thus, seahorses and pipefishes may be moving in the open ocean more than suspected, perhaps using floating mats of marine vegetation. If so, this behaviour could act as a hitherto unknown vector for syngnathid movement and dispersal. Information on syngnathid abundance in predator diet (measured as percent number, volume, or mass) was available in 45 reviewed accounts; in 27% (n = 12) of these studies seahorses or pipefishes comprised ≥20% of predator diet (range 0.005–100%). Frequency of occurrence (percent stomachs, seabird bill-loads, or regurgitations in which a prey item occurred) was provided in 39 accounts, with 15% (n = 6) of these recording a frequency of ≥20% (range 0.003–65%).     

Testes investment and spawning mode in pipefishes and seahorses (Syngnathidae)

Externally fertilizing fishes are predicted to invest heavily in testes, because large numbers of sperm should be favoured by the high risk of sperm competition from sneaker males, and/or the dilution of ejaculates when shed into open water. Using museum specimens, we measured testes mass and body mass of 83 mature males, belonging to 21 genera of the family Syngnathidae (pipefishes and seahorses). In this family all species show paternal care, ranging in degree from eggs being attached to the skin of the male, to eggs being completely enclosed and nurtured within a brood pouch. The former, 'unprotected' group, is thought to have external fertilization, whereas in the latter, 'protected' group, males fertilize the eggs internally in their brood pouch. Smaller relative testes investment was thus predicted for genera that have protected compared with unprotected brood care. However, we found this not to be the case. Instead, all genera showed the same relationship between testes and body mass, regardless of brooding type. The possible implications of this surprising result are discussed, including the possibility that the mode of fertilization might have been misjudged for the pouchless syngnathids.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 369–376.     

Modelling stress in the feeding apparatus of seahorses and pipefishes (Teleostei: Syngnathidae)

Seahorses and pipefishes are extremely fast suction feeders, and the fast strikes probably result in large and rapid pressure drops in the buccal cavity. These rapid drops in pressure imply heavy mechanical loading on the cranium; hence, the feeding apparatus is thought to experience high levels of stress. We used finite element analysis (FEA) to investigate where stress accumulates under strong suction pressure, and whether there is a difference in craniofacial stress distribution between long‐ and short‐snouted species. The expectation was that high stress levels would occur at the articulations and in the cartilaginous regions of the cranium, and that, given the same pressure, the skulls of long‐snouted species would exhibit lower stress levels than the skulls of short‐snouted species, as an evolutionary increase in snout length might have made these species structurally better adapted to deal with high suction pressures. The results partially support the first hypothesis: except for Dunckerocampus dactyliophorus, all models show peak stress concentrations at the articulations and cartilaginous regions. However, no simple relationship between snout length and the magnitudes of stress predicted by the FEA was found. In an attempt to explain this lack of a relationship, the methodology was evaluated by assessing the effect of hyoid position and model construction on the stress distribution. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 680–691.     

Mating portfolios: bet-hedging,sexual selection and female multiple mating

Polyandry (female multiple mating) has profound evolutionary and ecological implications. Despite considerable work devoted to understanding why females mate multiply, we currently lack convincing empirical evidence to explain the adaptive value of polyandry. Here, we provide a direct test of the controversial idea that bet-hedging functions as a risk-spreading strategy that yields multi-generational fitness benefits to polyandrous females. Unfortunately, testing this hypothesis is far from trivial, and the empirical comparison of the across-generations fitness payoffs of a polyandrous (bet hedger) versus a monandrous (non-bet hedger) strategy has never been accomplished because of numerous experimental constraints presented by most ‘model’ species. In this study, we take advantage of the extraordinary tractability and versatility of a marine broadcast spawning invertebrate to overcome these challenges. We are able to simulate multi-generational (geometric mean) fitness among individual females assigned simultaneously to a polyandrous and monandrous mating strategy. Our approaches, which separate and account for the effects of sexual selection and pure bet-hedging scenarios, reveal that bet-hedging, in addition to sexual selection, can enhance evolutionary fitness in multiply mated females. In addition to offering a tractable experimental approach for addressing bet-hedging theory, our study provides key insights into the evolutionary ecology of sexual interactions.     

Morphological variation in head shape of pipefishes and seahorses in relation to snout length and developmental growth

The feeding apparatus of Syngnathidae, with its elongate tubular snout and tiny, toothless jaws, is highly specialized for performing fast and powerful pivot feeding. In addition, the prolonged syngnathid parental care probably enables the juveniles to be provided with a feeding apparatus that resembles the one in adults, both in morphology and function. In this study, a landmark‐based geometric morphometric analysis was carried out on the head of syngnathid representatives in order to (1) examine to what degree pipefish shape variation is different from that of seahorses; (2) determine whether the high level of specialization reduces the amount of intraspecific morphological variation found within the family; and (3) elucidate whether or not important shape changes occur in the seahorse head during postrelease ontogeny. We found that (1) there is a significant shape difference between head shape of pipefish and seahorse: the main differences concern snout length and height, position and orientation of the pectoral fin base, and height of the head and opercular bone. We hypothesize that this might be related to different prey capture kinematics (long snout with little head rotation versus short snout with large head rotation) and to different body postures (in line with the head versus vertical with a tilted head) in pipefishes and seahorses; (2) both pipefishes and seahorses showed an inverse relation between relative snout length and intraspecific variation and although pipefishes show a large diversity in relative snout elongation, they are more constrained in terms of head shape; and (3) the head of juvenile Hippocampus reidi specimens still undergoes gradual shape changes after being expelled from the brood pouch. Ontogenetic changes include lowering of the snout and head but also differences in orientation of the preopercular bone and lowering of the snout tip. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

Mating preferences, sexual selection and patterns of cladogenesis in ray-finned fishes

Evolutionary theory predicts that sexual selection may increase taxonomic diversity when emergent mating preferences result in reproductive isolation and therefore speciation. This theory has been invoked to explain patterns of diversity in ray-finned fishes (most notably in the cichlids), but the theory has not been tested comparatively in fish. Additionally, several other unrelated factors have been identified as promoters of cladogenesis, so it is unclear how important sexual selection might be in diversification. Using sister-clade analysis, I tested the relationship between the presence of sexually selected traits and taxonomic diversification in actinopterygiian fishes, a large clade that shows substantial diversity in mating preferences and related sexually selected traits. In all identified sister-families that differed with regard to the proportion of species manifesting sexually selected traits, sexual selection was correlated with increased diversification, and this association was significant across all sister clades (P=0.02). This suggests that sexual selection, when present, is a substantial driver of diversification in the ray-finned fishes, and lends further empirical support to the theoretical link between mating preferences and accelerated cladogenesis.     

Mating system and demographic constraints on the opportunity for sexual selection

In monogamous systems the fitness difference between males due to competition for mates is limited to one female. This constraint presumably impedes the action of sexual selection relative to polygynous systems. In this paper, we use formal selection theory to show how population size and the adult sex ratio constrain the force of sexual selection and phenotypic evolution under monogamy and polygyny. The force of sexual selection is ultimately constrained by the number of males in a population and the theoretical limit to the rate of male phenotypic evolution is realized if a single male mates with one or many females. These results imply that the force of sexual selection is not strictly constrained by monogamy. The constraint on female phenotypic evolution is typically higher than the constraint on males under polygyny and similar to selection on males in monogamous systems. The sexual asymmetry in the force of selection under polygyny--not necessarily weak sexual selection on males of monogamous systems--may explain the prominence of sexual dimorphism in polygynous systems.     

Mating system, sexual dimorphism, and the opportunity for sexual selection in a territorial ungulate

In mammals, species with high sexual size dimorphism tend tohave highly polygynous mating systems associated with high variancein male lifetime reproductive success (LRS), leading to a highopportunity for sexual selection. However, little informationis available for species with weak sexual size dimorphism. Ina long-term study population, we used parentage analysis basedon 21 microsatellite markers to describe, for the first time,variance in male lifetime breeding success (LBS) of roe deer,a territorial ungulate where males weigh less than 10% morethan females. LBS ranged from 0 to 14 (mean = 4.54, variance= 15.5), and its distribution was highly skewed, with only afew males obtaining high LBS and many males failing to breedor siring only one fawn. As predicted for polygynous specieswith low sexual size dimorphism, the standardized variance inmale LBS was low (I_m = 0.75) and was only slightly higher thanthe standardized variance in female LRS (I_f = 0.53), suggestinga low opportunity for sexual selection. The I_m value reportedhere for roe deer is much lower than values reported for highlydimorphic ungulates such as red deer (I_m > 3). We suggestthat, along a continuum of opportunity for sexual selection,roe deer occupy a position closer to monogamous and monomorphicterritorial ungulates than to highly polygynous, sexually dimorphicungulates with dominance rank–based mating systems suchas harems or roving mating systems.     

Male pregnancy in seahorses and pipefishes (family Syngnathidae): rapid diversification of paternal brood pouch morphology inferred from a molecular phylogeny

In contrast to the majority of vertebrate species, primary male parental care is common in fishes and encompasses a remarkable diversity of adaptations. Seahorses and pipefishes (Family Syngnathidae) exhibit some of the most specialized forms of paternal care in animals and so are ideally suited to the study of the evolution of male parental care. During mating, female syngnathids transfer eggs to specialized morphological structures that are located on either the abdomen or tail of the male. The male provides all postfertilization parental care and has morphological and physiological adaptations to osmoregulate, aerate, and even nourish the developing embryos. While all syngnathid species are adapted for paternal care, the brooding structure with which this is accomplished varies between species, from simple ventral gluing areas to much more complex structures such as the completely enclosed pouches of the seahorses. Our combined cytochrome b-, 12S rDNA-, and 16S rDNA-based molecular phylogeny of syngnathid fishes demonstrates that rapid diversification of male brooding structures has been associated with the major evolutionary radiation of the group, suggesting that development and diversification of structures involved in paternal care may have been key evolutionary innovations of the Syngnathidae. Molecular analyses also highlight geographical centers of biodiversity and suggest interoceanic migration of Syngnathus pipefishes from their center of origin in the Pacific.     

Mating density and the strength of sexual selection against deleterious alleles in Drosophila melanogaster

Deleterious alleles constantly enter populations via mutation. Their presence reduces mean fitness and may threaten population persistence. It has been suggested that sexual selection may be an efficient way by which deleterious alleles are removed from populations but there is little direct experimental evidence. Because of its potential role in mutational meltdowns, there is particular interest in whether the strength of sexual selection changes with density. For each of eight visible markers in Drosophila melanogaster we have compared the strength of sexual selection at two densities. We find evidence of strong sexual selection against most but not all of these alleles. There is no evidence that sexual selection tends to be stronger (or weaker) at high density relative to low density. In addition, we also measure the effects of these mutations on two key parameters relevant to population productivity--juvenile viability and female fecundity. In most cases, sexual selection is as strong or stronger than these other forms of selection.