Melissah Rowe

Sperm Competition Selects for Sperm Quantity and Quality in the Australian Maluridae

When ejaculates from rival males compete for fertilization, there is strong selection for sperm traits that enhance fertilization success. Sperm quantity is one such trait, and numerous studies have demonstrated a positive association between sperm competition and both testes size and the number of sperm available for copulations. Sperm competition is also thought to favor increases in sperm quality and changes in testicular morphology that lead to increased sperm production. However, in contrast to sperm quantity, these hypotheses have received considerably less empirical support and remain somewhat controversial. In a comparative study using the Australian Maluridae (fairy-wrens, emu-wrens, grasswrens), we tested whether increasing levels of sperm competition were associated with increases in both sperm quantity and quality, as well as an increase in the relative amount of seminiferous tubule tissue contained within the testes. After controlling for phylogeny, we found positive associations between sperm competition and sperm numbers, both in sperm reserves and in ejaculate samples. Additionally, as sperm competition level increased, the proportion of testicular spermatogenic tissue also increased, suggesting that sperm competition selects for greater sperm production per unit of testicular tissue. Finally, we also found that sperm competition level was positively associated with multiple sperm quality traits, including the proportion of motile sperm in ejaculates and the proportion of both viable and morphologically normal sperm in sperm reserves. These results suggest multiple ejaculate traits, as well as aspects of testicular morphology, have evolved in response to sperm competition in the Australian Maluridae. Furthermore, our findings emphasize the importance of post-copulatory sexual selection as an evolutionary force shaping macroevolutionary differences in sperm phenotype.

Plumage coloration, ejaculate quality and reproductive phenotype in the red-backed fairy-wren

Understanding how pre- and postcopulatory sexually selected traits covary can provide insight into the evolution of male ornamentation and female mate choice. In this study, we examined ejaculate quality and investment in testicular tissue in relation to plumage colour and social status in the genetically promiscuous red-backed fairy-wren, Malurus melanocephalus. In this species, males exhibit one of three alternative reproductive phenotypes during the breeding season: males can breed in red and black plumage, breed in brown plumage, or act as brown-plumed, nonbreeding auxiliaries. We found that red/ black breeders invested more heavily in spermatogenic tissue, had larger sperm reserves, and tended to have greater numbers of sperm in ejaculate samples, when compared to brown breeders and auxiliaries. Within red/black breeders, plumage redness and saturation (i.e. long wavelength hue and increased red chroma) were negatively correlated with ejaculate sample sperm density. In addition, ejaculate motility appeared to be related to variation in plumage coloration such that, overall, males with less elaborate ornamentation showed greater ejaculate quality. These results suggest that pre- and postcopulatory traits negatively covary in red/black plumed red-backed fairy-wrens and indicate a possible trade-off between investment in plumage ornaments and investment in ejaculates.

Ontogenetic immune challenges shape adult personality in mallard ducks

Consistent individual differences in behaviour are widespread in animals, but the proximate mechanisms driving these differences remain largely unresolved. Parasitism and immune challenges are hypothesized to shape the expression of animal personality traits, but few studies have examined the influence of neonatal immune status on the development of adult personality. We examined how non-pathogenic immune challenges, administered at different stages of development, affected two common measures of personality, activity and exploratory behaviour, as well as colour-dependent novel object exploration in adult male mallard ducks (Anas platyrhynchos). We found that individuals that were immune-challenged during the middle (immediately following the completion of somatic growth) and late (during the acquisition of nuptial plumage) stages of development were more active in novel environments as adults relative to developmentally unchallenged birds or those challenged at an earlier developmental time point. Additionally, individuals challenged during the middle stage of development preferred orange and avoided red objects more than those that were not immune-challenged during development. Our results demonstrate that, in accordance with our predictions, early-life immune system perturbations alter the expression of personality traits later in life, emphasizing the role that developmental plasticity plays in shaping adult personality, and lending support to recent theoretical models that suggest that parasite pressure may play an important role in animal personality development.

POSTCOPULATORY SEXUAL SELECTION INCREASES ATP CONTENT IN RODENT SPERMATOZOA

Sperm competition often leads to increase in sperm numbers and sperm quality, and its effects on sperm function are now beginning to emerge. Rapid swimming speeds are crucial for mammalian spermatozoa, because they need to overcome physical barriers in the female tract, reach the ovum, and generate force to penetrate its vestments. Faster velocities associate with high sperm competition levels in many taxa and may be due to increases in sperm dimensions, but they may also relate to higher adenosine triphosphate (ATP) content. We examined if variation in sperm ATP levels relates to both sperm competition and sperm swimming speed in rodents. We found that sperm competition associates with variations in sperm ATP content and sperm‐size adjusted ATP concentrations, which suggests proportionally higher ATP content in response to sperm competition. Moreover, both measures were associated with sperm swimming velocities. Our findings thus support the idea that sperm competition may select for higher ATP content leading to faster sperm swimming velocity.

Carotenoids in the Seminal Fluid of Wild Birds: Interspecific Variation in Fairy-Wrens

Abstract Male secondary sexual characters can provide females with information regarding the fertilizing capacity of a males sperm. In some fishes and birds, intense nuptial coloration is correlated with male fertilizing capacity, but no mechanistic link between coloration and sperm quality has been established. One plausible mechanism is that carotenoid pigments, which color skin and feathers in many animals, are present in seminal fluid and serve as antioxidant protectors of sperm. We used high-performance liquid chromatography (HPLC) to analyze sperm samples from four species of Australian fairy-wren (Malurus) and detected low concentrations (<1 μg ml−1) of carotenoids in some samples. Xanthophyll carotenoids (including lutein and zeaxanthin), which are typically dietary in origin, were present in the seminal fluid of Superb (M. cyaneus) and Splendid (M. splendens) Fairy-Wrens. In contrast, red ketocarotenoids (including astaxanthin and canthaxanthin), which are likely metabolically derived from dietary precursors, were present in the seminal fluid of Red-backed Fairy-Wrens (M. melanocephalus). This work is the first to report carotenoids in avian seminal fluid and suggests that, although carotenoids are at low levels and thus may have limited antioxidant activity, there may be biological variability in avian semen carotenoids on which selection could act.

Evolution of sperm structure and energetics in passerine birds

Spermatozoa exhibit considerable interspecific variability in size and shape. Our understanding of the adaptive significance of this diversity, however, remains limited. Determining how variation in sperm structure translates into variation in sperm performance will contribute to our understanding of the evolutionary diversification of sperm form. Here, using data from passerine birds, we test the hypothesis that longer sperm swim faster because they have more available energy. We found that sperm with longer midpieces have higher levels of intracellular adenosine triphosphate (ATP), but that greater energy reserves do not translate into faster-swimming sperm. Additionally, we found that interspecific variation in sperm ATP concentration is not associated with the level of sperm competition faced by males. Finally, using Bayesian methods, we compared the evolutionary trajectories of sperm morphology and ATP content, and show that both traits have undergone directional evolutionary change. However, in contrast to recent suggestions in other taxa, we show that changes in ATP are unlikely to have preceded changes in morphology in passerine sperm. These results suggest that variable selective pressures are likely to have driven the evolution of sperm traits in different taxa, and highlight fundamental biological differences between taxa with internal and external fertilization, as well as those with and without sperm storage.

Postcopulatory sexual selection is associated with accelerated evolution of sperm morphology

Rapid diversification of sexual traits is frequently attributed to sexual selection, though explicit tests of this hypothesis remain limited. Spermatozoa exhibit remarkable variability in size and shape, and studies report a correlation between sperm morphology (sperm length and shape) and sperm competition risk or female reproductive tract morphology. However, whether postcopulatory processes (e.g., sperm competition and cryptic female choice) influence the speed of evolutionary diversification in sperm form is unknown. Using passerine birds, we quantified evolutionary rates of sperm length divergence among lineages (i.e., species pairs) and determined whether these rates varied with the level of sperm competition (estimated as relative testes mass). We found that relative testes mass was significantly and positively associated with more rapid phenotypic divergence in sperm midpiece and flagellum lengths, as well as total sperm length. In contrast, there was no association between relative testes mass and rates of evolutionary divergence in sperm head size, and models suggested that head length is evolutionarily constrained. Our results are the first to show an association between the strength of sperm competition and the speed of sperm evolution, and suggest that postcopulatory sexual selection promotes rapid evolutionary diversification of sperm morphology.

Extra-pair paternity, sperm competition and their evolutionary consequences in the Maluridae

Abstract Fairy-wrens (Malurus) are socially monogamous and yet exhibit among the highest rates of extra-pair paternity (EPP) known in passerine birds. Here, we review patterns of EPP in fairy-wrens and their allies (Maluridae), and discuss the causes and evolutionary consequences of multiple mating in this group. Rates of EPP vary widely across species, but correlate strongly with relative testes mass suggesting that testes mass can be used as a proxy for EPP in comparative studies. With respect to variation in EPP, there appear to be consistent habitat differences between the subfamilies of Maluridae that may contribute to the observed inter-specific variation in rates of EPP, and specific habitat requirements of some species may influence patterns of paternity between species of Malurus. Within species, however, there is equivocal evidence for a role of group size influencing rates of EPP. Regardless of the causes of variation in EPP, available evidence suggests that female fairy-wrens may benefit from extra-pair matings through indirect genetic benefits, such as inbreeding avoidance and choice of high-quality males (i.e. good genes). Using Bayesian modelling, we show that the ancestral state in Australian malurids is one of low sperm competition, and that, in general, increased levels of sperm competition (and hence EPP) are a derived condition in this family. Given the broad range of levels of sperm competition in this family and the relationship between relative testes mass and EPP, we suggest that the Maluridae are a model system for studies of EPP and sperm competition.

Patterns of sperm damage in Chernobyl passerine birds suggest a trade-off between sperm length and integrity

Interspecific variation in sperm size is enigmatic, but generally assumed to reflect species-specific trade-offs in selection pressures. Among passerine birds, sperm length varies sevenfold, and sperm competition risk seems to drive the evolution of longer sperm. However, little is known about factors favouring short sperm or constraining the evolution of longer sperm. Here, we report a comparative analysis of sperm head abnormalities among 11 species of passerine bird in Chernobyl, presumably resulting from chronic irradiation following the 1986 accident. Frequencies of sperm abnormalities varied between 15.7 and 77.3% among species, more than fourfold higher than in uncontaminated areas. Nonetheless, species ranked similarly in sperm abnormalities in unpolluted areas as in Chernobyl, pointing to intrinsic factors underlying variation in sperm damage among species. Scanning electron microscopy of abnormal spermatozoa revealed patterns of acrosome damage consistent with premature acrosome reaction. Sperm length, but not sperm competition risk explained variation in sperm damage among species. This suggests that longer spermatozoa are more susceptible to premature acrosome reaction. Therefore, we hypothesize a trade-off between sperm length and sperm integrity affecting sperm evolution in passerine birds.

Commonness and ecology, but not bigger brains, predict urban living in birds

BackgroundSeveral life history and ecological variables have been reported to affect the likelihood of species becoming urbanized. Recently, studies have also focused on the role of brain size in explaining ability to adapt to urban environments. In contrast, however, little is known about the effect of colonization pressure from surrounding areas, which may confound conclusions about what makes a species urban. We recorded presence/absence data for birds in 93 urban sites in Oslo (Norway) and compared these with species lists generated from 137 forest and 51 farmland sites surrounding Oslo which may represent source populations for colonization.ResultsWe found that the frequency (proportion of sites where present) of a species within the city was strongly and positively associated with its frequency in sites surrounding the city, as were both species breeding habitat and nest site location. In contrast, there were generally no significant effects of relative brain mass or migration on urban occupancy. Furthermore, analyses of previously published data showed that urban density of birds in six other European cities was also positively and significantly associated with density in areas outside cities, whereas relative brain mass showed no such relationship.ConclusionsThese results suggest that urban bird communities are primarily determined by how frequently species occurred in the surrounding landscapes and by features of ecology (i.e. breeding habitat and nest site location), whereas species’ relative brain mass had no significant effects.