The mating brain: early maturing sneaker males maintain investment into the brain also under fast body growth in Atlantic salmon (Salmo salar)

It has been suggested that mating behaviours require high levels of cognitive ability. However, since investment into mating and the brain both are costly features, their relationship is likely characterized by energetic trade-offs. Empirical data on the subject remains equivocal. We investigated if early sexual maturation was associated with brain development in Atlantic salmon (Salmo salar), in which males can either stay in the river and sexually mature at a small size (sneaker males) or migrate to the sea and delay sexual maturation until they have grown much larger (anadromous males). Specifically, we tested how sexual maturation may induce plastic changes in brain development by rearing juveniles on either natural or ad libitum feeding levels. After their first season we compared brain size and brain region volumes across both types of male mating tactics and females. Body growth increased greatly across both male mating tactics and females during ad libitum feeding as compared to natural feeding levels. However, despite similar relative increases in body size, early maturing sneaker males maintained larger relative brain size during ad libitum feeding levels as compared to anadromous males and females. We also detected several differences in the relative size of separate brain regions across feeding treatments, sexes and mating strategies. For instance, the relative size of the cognitive centre of the brain, the telencephalon, was largest in sneaker males. Our data support that a large relative brain size is maintained in individuals that start reproduction early also during fast body growth. We propose that the cognitive demands during complex mating behaviours maintain a high level of investment into brain development in reproducing individuals.     

Sexual selection impacts brain anatomy in frogs and toads

Natural selection is a major force in the evolution of vertebrate brain size, but the role of sexual selection in brain size evolution remains enigmatic. At least two opposing schools of thought predict a relationship between sexual selection and brain size. Sexual selection should facilitate the evolution of larger brains because better cognitive abilities may aid the competition for mates. However, it may also restrict brain size evolution due to energetic trade‐offs between brain tissue and sexually selected traits. Here, we examined the patterns of selection on brain size and brain anatomy in male anurans (frogs and toads), a group where the strength of sexual selection differs markedly among species, using a phylogenetically controlled generalized least‐squared (PGLS) regression analyses. The analysis revealed that in 43 Chinese anuran species, neither mating system, nor type of courtship, or testes mass was significantly associated with relative brain size. While none of those factors related to the relative size of olfactory nerves, optic tecta, telencephalon, and cerebellum, the olfactory bulbs were relatively larger in monogamous species and those using calls during courtship. Our findings support the mosaic model of brain evolution and suggest that while the investigated aspects of sexual selection do not seem to play a prominent role in the evolution of brain size of anurans, they do impact their brain anatomy.     

On the evolution of brain size in relation to migratory behaviour in birds

Migratory birds appear to have relatively smaller brain size compared to sedentary species. It has been hypothesized that initial differences in brain size underlying behavioural flexibility drove the evolution of migratory behaviour; birds with relatively large brains evolved sedentary habits and those with relatively small brains evolved migratory behaviour (migratory precursor hypothesis). Alternative hypotheses suggest that changes in brain size might follow different behavioural strategies and that sedentary species might have evolved larger brains because of differences in selection pressures on brain size in migratory and nonmigratory species. Here we present the first evidence arguing against the migratory precursor hypothesis. We compared relative brain volume of three subspecies of the white-crowned sparrow: sedentary Zonotrichia leucophrys nuttalli and migratory Z. l. gambelii and Z. l. oriantha. Within the five subspecies of the white-crowned sparrow, only Z. l. nuttalli is strictly sedentary. The sedentary behaviour of Z. l. nuttalli is probably a derived trait, because Z. l. nuttalli appears to be the most recent subspecies and because all species ancestral to Zonotrichia as well as all older subspecies of Z. leucophrys are migratory. Compared to migratory Z. l. gambelii and Z. l. oriantha, we found that sedentary Z. l. nuttalli had a significantly larger relative brain volume, suggesting that the larger brain of Z. l. nuttalli evolved after a switch to sedentary behaviour. Thus, in this group, brain size does not appear to be a precursor to the evolution of migratory or sedentary behaviour but rather an evolutionary consequence of a change in migratory strategy.     

Sexual bimaturation and sexual size dimorphism in animals with asymptotic growth after maturity

Many animal taxa exhibit a positive correlation between sexual size dimorphism and sex differences in age at maturity, such that members of the larger sex mature at older ages than members of the smaller sex. Previous workers have suggested that sexual bimaturation is a product of sex differences in growth trajectories, but to date no one has tested this hypothesis. The current study uses growth-based models to study relationships between sexual size dimorphism and sexual bimaturation in species with asymptotic growth after maturity. These models show that sex differences in asymptotic size would produce sexual bimaturation even if both sexes approach their respective asymptotic sizes at the same age, mature at the same proportion of asymptotic size and have otherwise equivalent growth and maturation patterns. Furthermore, our analyses show that there are three ways to reduce sexual bimaturation in sexually size-dimorphic species: (1) higher characteristic growth rates for members of the larger sex, (2) larger size at birth, hatching or metamorphosis for members of the larger sex or (3) smaller ratio of size at maturity to asymptotic size (relative size at maturity) for members of the larger sex. Of these three options, sex differences in relative size at maturity are most common in size-dimorphic species and, in both male-larger and female-larger species, members of the larger sex frequently mature at a smaller proportion of their asymptotic size than do members of the smaller sex. Information about the growth and maturation patterns of a taxon can be used to determine relationships between sexual size dimorphism and sexual bimaturation for the members of that taxon. This process is illustrated for Anolis lizards, a genus in which both sexes exhibit the same strong correlation (r 0.97) between size at maturity and asymptotic size, and in which the relative size at maturity is inversely related to asymptotic size for both sexes. As a result, sexually size-dimorphic species of anoles exhibit the expected pattern of a smaller relative size at maturity for members of the larger sex. However, for species in this genus, sex differences in the relative size at maturity are not strong enough to produce the same age at maturity for both sexes in sexually size-dimorphic species. Members of the larger sex (usually males) are still expected to mature at older ages than members of the smaller sex in Anolis lizards.     

Coordinated evolution of brain size,structure, and eye size in Trinidadian killifish

Brain size, brain architecture, and eye size vary extensively in vertebrates. However, the extent to which the evolution of these components is intricately connected remains unclear. Trinidadian killifish, Anablepsoides hartii, are found in sites that differ in the presence and absence of large predatory fish. Decreased rates of predation are associated with evolutionary shifts in brain size; males from sites without predators have evolved a relatively larger brain and eye size than males from sites with predators. Here, we evaluated the extent to which the evolution of brain size, brain structure, and eye size covary in male killifish. We utilized wild‐caught and common garden‐reared specimens to determine whether specific components of the brain have evolved in response to differences in predation and to determine if there is covariation between the evolution of brain size, brain structure, and eye size. We observed consistent shifts in brain architecture in second generation common garden reared, but not wild caught preserved fish. Male killifish from sites that lack predators exhibited a significantly larger telencephalon, optic tectum, cerebellum, and dorsal medulla when compared with fish from sites with predators. We also found positive connections between the evolution of brain structure and eye size but not between overall brain size and eye size. These results provide evidence for evolutionary covariation between the components of the brain and eye size. Such results suggest that selection, directly or indirectly, acts upon specific regions of the brain, rather than overall brain size, to enhance visual capabilities.     

Sex, ecology and the brain: evolutionary correlates of brain structure volumes in Tanganyikan cichlids

Analyses of the macroevolutionary correlates of brain structure volumes allow pinpointing of selective pressures influencing specific structures. Here we use a multiple regression framework, including phylogenetic information, to analyze brain structure evolution in 43 Tanganyikan cichlid species. We analyzed the effect of ecological and sexually selected traits for species averages, the effect of ecological traits for each sex separately and the influence of sexual selection on structure dimorphism. Our results indicate that both ecological and sexually selected traits have influenced brain structure evolution. The patterns observed in males and females generally followed those observed at the species level. Interestingly, our results suggest that strong sexual selection is associated with reduced structure volumes, since all correlations between sexually selected traits and structure volumes were negative and the only statistically significant association between sexual selection and structure dimorphism was also negative. Finally, we previously found that monoparental female care was associated with increased brain size. However, here cerebellum and hypothalamus volumes, after controlling for brain size, associated negatively with female-only care. Thus, in accord with the mosaic model of brain evolution, brain structure volumes may not respond proportionately to changes in brain size. Indeed selection favoring larger brains can simultaneously lead to a reduction in relative structure volumes.     

Evolution of brain region volumes during artificial selection for relative brain size

The vertebrate brain shows an extremely conserved layout across taxa. Still, the relative sizes of separate brain regions vary markedly between species. One interesting pattern is that larger brains seem associated with increased relative sizes only of certain brain regions, for instance telencephalon and cerebellum. Till now, the evolutionary association between separate brain regions and overall brain size is based on comparative evidence and remains experimentally untested. Here, we test the evolutionary response of brain regions to directional selection on brain size in guppies (Poecilia reticulata) selected for large and small relative brain size. In these animals, artificial selection led to a fast response in relative brain size, while body size remained unchanged. We use microcomputer tomography to investigate how the volumes of 11 main brain regions respond to selection for larger versus smaller brains. We found no differences in relative brain region volumes between large‐ and small‐brained animals and only minor sex‐specific variation. Also, selection did not change allometric scaling between brain and brain region sizes. Our results suggest that brain regions respond similarly to strong directional selection on relative brain size, which indicates that brain anatomy variation in contemporary species most likely stem from direct selection on key regions.     

Alternative mating strategies in Atlantic salmon and brown trout

By screening variable number of tandem repeat (VNTR) loci, multiple paternity within clutches has been found in wild populations of southern European Atlantic salmon (Salmo salar) and brown trout (Salmo trutta). For Atlantic salmon, we determined the relative contribution of alternative male phenotypes to the next generation. Individual males that are morphologically juvenile yet sexually mature fertilized a large proportion of eggs, and they thereby contributed to an increase of genetic variability in wild populations via (1) balancing the sex ratio, (2) increasing outbreeding, and (3) enlarging the effective population size, in part a consequence of (1) and (2). In addition, these precocious males ensured that interspecific spawns involving Atlantic salmon females and brown trout males (a fairly common occurrence in southern Europe where the two species are sympatric) resulted mostly in Atlantic salmon progeny. For brown trout, preliminary genetic results indicated that multiple paternity, when present, was not due to alternative mating strategies by males, but rather to successive fertilizations by adult suitors.     

Using testis size to predict the mating systems of New Zealand geckos

Abstract

The mating system is unknown for the majority of New Zealand geckos (Family Gekkonidae). I investigated interspecific variation in relative testis volume across 19 New Zealand gecko taxa and 63 additional species of squamate reptiles from other countries to make predictions about the social mating system of the New Zealand geckos. Relative testis size varied greatly between species of New Zealand gecko, with testes ranging from 119% larger than expected to 75% smaller than expected. This variation was even greater across other squamates, with testes ranging from 55 to 152% of expected size. This variation could not be explained by seasonality of breeding, clutch size or the sex ratio of populations. As species subject to more intense sperm competition sport relatively larger testes in other vertebrate groups, it is likely that similar variation in gecko testis size is due to differences in mating systems between species. Based on testis volume, it is predicted that at least half of the New Zealand gecko taxa studied are likely to have polygynandrous mating systems.     

Protandrous migration and variation in morphological characters in Emberiza buntings at an East Asian stopover site

The effect of the timing of spring migration on reproductive success differs between the sexes. As a consequence, various sex‐specific tactics relating to the timing of migration have evolved in migratory avian groups. Various hypotheses have been proposed to explain differential migration to breeding or wintering grounds, and inter‐ and intrasexual size differences are often considered one of the proximate mechanisms. We investigated arrival patterns in the spring by individuals of each sex, sexual size dimorphism and related morphological variables, and the relationship between size variation and arrival date in five bunting species that passed through an East Asian migratory flyway stopover site in 2006–08. Males of all the study species arrived before females, and significant sexual dimorphism was observed. Several morphological characters, including total length, wing‐length and tail‐length, contributed to the size variation. Although larger males arrived earlier, there was no relationship between arrival date and size in females. Our study confirmed that East Asian buntings display a discriminated protandrous migration pattern at the stopover site as well as at the breeding grounds. This is consistent with the view that larger body size in males is favoured due to its association with early arrival to help ensure access to the best resources and hence enhanced mating success.     

Life histories of closely related amphidromous and non‐migratory fish species: a trade‐off between egg size and fecundity

相似文献   

Predation pressure shapes brain anatomy in the wild

There is remarkable diversity in brain anatomy among vertebrates and evidence is accumulating that predatory interactions are crucially important for this diversity. To test this hypothesis, we collected female guppies (Poecilia reticulata) from 16 wild populations and related their brain anatomy to several aspects of predation pressure in this ecosystem, such as the biomass of the four major predators of guppies (one prawn and three fish species), and predator diversity (number of predatory fish species in each site). We found that populations from localities with higher prawn biomass had relatively larger telencephalon size as well as larger brains. Optic tectum size was positively associated with one of the fish predator’s biomass and with overall predator diversity. However, both olfactory bulb and hypothalamus size were negatively associated with the biomass of another of the fish predators. Hence, while fish predator occurrence is associated with variation in brain anatomy, prawn occurrence is associated with variation in brain size. Our results suggest that cognitive challenges posed by local differences in predator communities may lead to changes in prey brain anatomy in the wild.     

Ecological context and the importance of body and gnathopod size for pairing success in two amphipod ecomorphs

Ecological context generates interspecific variation in mating behavior by imposing differential constraints on the action of sexual selection, but operation of these constraints in nature is not well understood. We used field and laboratory studies to examine the importance of body size and size of sexually dimorphic appendages, the gnathopods, for pairing success in two freshwater amphipod species within the Hyalella azteca species complex. We focused on a large-bodied species found in habitats where ecological factors tend to favor large body size, and a small-bodied species in habitats where small body size is favored by size-selective predation. A field study indicated that although male pairing success was greater for larger males in both species, pairing success increased throughout the range of variation in male size in the large species, whereas, in the small species, pairing success was low for smaller individuals, but roughly constant across intermediate to larger sizes. A laboratory mate choice experiment was consistent with the field study, finding that females of the large species exhibited a preference for larger males that was independent of absolute male size, but females of the small species were indifferent when choosing between males of intermediate to larger size. Species also differed in the direction of sexual size dimorphism in the field, with males being the larger sex in the large species but the smaller sex in the small species, a pattern consistent with the species differences in mate preference. Large gnathopod size relative to body size was associated with enhanced pairing success across all body sizes for the large species, but, in the small species, large gnathopod size enhanced pairing success only in smaller males. Species differences in mating behavior appear consistent with change driven by differing forms of the interaction between sexual and natural selection.     

Sexual selection and the brain

Sex differences are intrinsically interesting, particularly in the brain. When sexually dimorphic structures mediate learning, and when such learning ability is necessary to compete for mates, then such differences are best understood within the framework of sexual selection. By categorizing recent studies of sex differences in the brain by their role in mate competition, theories of sexual selection can be used to predict and characterize the occurrence of dimorphisms among species with different mating systems.     

Genital morphology and allometry differ by species and sex in Malawi cichlid fishes

The African cichlid fishes show great diversity in mating displays and reproductive strategies, yet species differences in genital morphology have been little studied. Observational notes have described broad sex differences in external genital shape between males and females, but these differences have not been quantified. We examined three aspects of genital morphology (relative anogenital distance, relative vent length, and relative external genital area) in two riverine and eleven Lake Malawi African cichlid species from eight genera. We find the most sexually distinct morphology in the Lake Malawi rock cichlids and the least sexual dimorphism in the riverine outgroup; additionally, diversity in metrics within genus indicates that these traits are recently evolving. Sexual dimorphism in morphology is present in most species, and, in the Lake Malawi species, multivariate discriminant analysis allows for accurate assignment of gonadal sex based on genital morphology and body size. This will serve as a useful method for sexing fish in a nonlethal fashion and provides a starting point for further examination of the evolution of genital morphology in this diverse group of fishes.     

Sex differences in behaviour as an indirect consequence of mating system

A considerable literature has been devoted to documenting differences between the sexes. However, relatively little attention has hitherto been directed towards those differences that arise as an indirect consequence of mating system even though they can have profound implications for the daily lives of the animals involved. In this review we focus on differences in the non-reproductive behaviour of fish and relate these to sexual dimorphism in size and morphology, and to variance in fitness between the sexes. In line with our expectation, differences in distributional ecology, schooling, aggression, predator avoidance and foraging are exaggerated in sexually dimorphic species and polygamous mating systems. Nonetheless, the behaviour of males and females may also differ in sexually monomorphic and monogamous species. We conclude by highlighting promising directions for further research.     

Sex differences in spatial cognition in an invertebrate: the cuttlefish

Evidence of sex differences in spatial cognition have been reported in a wide range of vertebrate species. Several evolutionary hypotheses have been proposed to explain these differences. The one best supported is the range size hypothesis that links spatial ability to range size. Our study aimed to determine whether male cuttlefish (Sepia officinalis; cephalopod mollusc) range over a larger area than females and whether this difference is associated with a cognitive dimorphism in orientation abilities. First, we assessed the distance travelled by sexually immature and mature cuttlefish of both sexes when placed in an open field (test 1). Second, cuttlefish were trained to solve a spatial task in a T-maze, and the spatial strategy preferentially used (right/left turn or visual cues) was determined (test 2). Our results showed that sexually mature males travelled a longer distance in test 1, and were more likely to use visual cues to orient in test 2, compared with the other three groups. This paper demonstrates for the first time a cognitive dimorphism between sexes in an invertebrate. The data conform to the predictions of the range size hypothesis. Comparative studies with other invertebrate species might lead to a better understanding of the evolution of cognitive dimorphism.     

Within‐Species Mate Preferences Do Not Contribute to the Maintenance of Sexually Monomorphic Mating Signals in Green Lacewings

We know much less about the evolutionary forces and constraints that maintain similar mating displays in females and males than we do about sexually dimorphic mating displays. Both female and male green lacewings have sexually monomorphic vibrational mating signals and are equally choosy against heterospecific mating signals. This similarity in between‐species sex roles may explain a large part of the presence of species‐specific female signals in these species, but does not necessarily predict why female and male signals are similar. We tested for within‐species sex‐specific similarities in mate preferences in Chrysoperla lucasina that may contribute to the maintenance of sexually monomorphic mating signals in this species. We found weak preferences and low levels of discrimination for signals with varying fine‐scale temporal features (volley duration, period, and volley‐duty cycle). The longer signals that both sexes produced in response to playback were sexually monomorphic, but some females and most males also produced shorter signals with significantly reduced volley durations and periods. Notably, all of these signals had indistinguishable volley‐duty cycles, the ratio of volley duration to volley period. We propose that mating signals in C. lucasina are maintained in both sexes because of similar between‐species mate preferences, but the sexually monomorphic mating signals cannot be attributed to significant within‐species mate preferences. What differences are present in within‐species sex roles may be resolved by a male‐biased signal polymorphism, in long and short signals that are hypothesized to have distinct functions during mate calling and courtship.     

Effects of body size on sex‐related migration vary between two closely related gull species with similar size dimorphism

Studies of migration have revealed multiple trade‐offs with other life‐history traits that may underlie observed variation in migratory properties among ages and sexes. To assess whether, and to what extent, body size and/or sex‐specific differences in competition for resources (e.g. breeding territories or winter food) may shape variation in migration distance and timing of arrival in ecologically and phylogenetically related species, we combined over 30 000 sightings of individually marked, sexually mature males and females of Herring Gulls Larus argentatus and Lesser Black‐Backed Gulls Larus fuscus with biometric measurements and phenological observations at a mixed breeding colony. In L. argentatus, larger males migrated further from the breeding colony, whereas migration distance was independent of body size in adult females. In L. fuscus, no relationship between body size and migration distance was apparent in either sex. Mean arrival dates at the breeding colony did not vary with migration distances but differed between males and females of L. argentatus (but not L. fuscus). As allometry at least partly explains sexual segregation in migration behaviour in L. argentatus, but not in L. fuscus, we conclude that the effect of body size on sex‐related migratory strategies may vary between closely related, sympatric species despite similar size dimorphism.     

The influence of precocious sexual maturation on survival to adulthood of river stocked Baltic salmon, Salmo salar, smolts

During three consequtive years, 1975–1977, Individually tagged Baltic salmon Salmo salar smolts of sexually immature male and female fish (n = 35027, mean size: 15.2 cm) and precocious males (n = 6518, mean size: 14.2 cm) were released into Umeälven (Ume river), northern Sweden. Rate of survival (% captured adults) based on 3714 recoveries was significantly higher (p < 0.01) for smolts from immature fish (10.2%) than those from smolts of early maturing males, i.e. precocious males (2.2%). corresponding to an average yield of 474 and 85 kg per KHX) smolts released, respectively. Gain in survival was on average 2.5% and 1.4% per cm increase in smolt size for immature smolts and smolts from precocious males, respectively. The poor survival among smolts of precocious males is suggested to he related to an interaction between sexual maturation and smolting linked to incompletely resorbed gonads leading to a non migratory behaviour. These non migratory males are then suggested to suffer heavily by predation in the river.
The two smolt categories had a similar growth pattern in sea. Smolts from precocious males did not mature early in sea indicating no relation to grisling, i.e. sexually maturing fish returning after first winter in sea. Adult weight of fish returning the fourth summer after release was related to smolt size (P < 0.05). Our Response Surface Model (RSA) predicted that large smolts (19.0 cm) had a higher specific growth rate over their life-span compared to small smolts (<15.0 cm), 0.86% d⁻¹ and 0.46% d⁻¹, respectively. Large smolts (19.0 cm) attained a size of 3.0 kg during their second winter in sea about six months earlier than small smolts (13.0 cm). The paper discusses alternative release strategies that can be employed if the ultimate goal of salmon stocking is maximizing yield.