Robert C. Brooks

Experimental evidence that high levels of inbreeding depress sperm competitiveness

The effects of inbreeding on sperm quantity and quality are among the most dramatic examples of inbreeding depression. The extent to which inbreeding depression results in decreased fertilization success of a male’s sperm, however, remains largely unknown. This task is made more difficult by the fact that other factors, such as cryptic female choice, male sperm allocation and mating order, can also drive patterns of paternity. Here, we use artificial insemination to eliminate these extraneous sources of variation and to measure the effects of inbreeding on the competitiveness of a male’s sperm. We simultaneously inseminated female guppies (Poecilia reticulata) with equal amounts of sperm from an outbred (f = 0) male and either a highly (f = 0.59) or a moderately inbred (f = 0.25) male. Highly inbred males sired significantly fewer offspring than outbred males, but share of paternity did not differ between moderately inbred and outbred males. These findings therefore confirm that severe inbreeding can impair the competitiveness of sperm, but suggest that in the focal population inbreeding at order of a brother–sister mating does not reduce a male’s sperm competitiveness.

Physiological adaptations to reproduction. I. Experimentally increasing litter size enhances aspects of antioxidant defence but does not cause oxidative damage in mice

SUMMARY Life history theory suggests that investment in reproduction can trade off against growth, longevity and both reproduction and performance later in life. One possible reason for this trade-off is that reproduction directly causes somatic damage. Oxidative stress, an overproduction of reactive oxygen species in relation to cellular defences, can correlate with reproductive investment and has been implicated as a pathway leading to senescence. This has led to the suggestion that this aspect of physiology could be an important mechanism underlying the trade-off between reproduction and lifespan. We manipulated female reproductive investment to test whether oxidative stress increases with reproduction in mice. Each females pups were cross-fostered to produce litters of either two or eight, representing low and high levels of reproductive investment for wild mice. No differences were observed between reproductive groups at peak lactation for several markers of oxidative stress in the heart and gastrocnemius muscle. Surprisingly, oxidative damage to proteins was lower in the livers of females with a litter size of eight than in females with two pups or non-reproductive control females. While protein oxidation decreased, activity levels of the antioxidant enzyme superoxide dismutase increased in the liver, suggesting this may be one pathway used to protect against oxidative stress. Our results highlight the need for caution when interpreting correlative relationships and suggest that oxidative stress does not increase with enhanced reproductive effort during lactation.

The juvenile social environment introduces variation in the choice and expression of sexually selected traits

The juvenile environment provides numerous cues of the intensity of competition and the availability of mates in the near environment. As research demonstrates that the developing individuals can use these cues to alter their developmental trajectories, and therefore, adult phenotypes, we examined whether social cues available during development can affect the expression and the preference of sexually selected traits. To examine this, we used the Australian black field cricket (Telogryllus commodus), a species where condition at maturity is known to affect both male calling effort and female choice. We mimicked different social environments by rearing juveniles in two different densities crossed with three different calling environments. We demonstrate that the social environment affected female response speed but not preference, and male age-specific calling effort (especially the rate of senescence in calling effort) but not the structural/temporal parameters of calls. These results demonstrate that the social environment can introduce variation in sexually selected traits by modifying the behavioral components of male production and female choice, suggesting that the social environment may be an overlooked source of phenotypic variation. We discuss the plasticity of trait expression and preference in reference to estimations of male quality and the concept of condition dependence.

The importance of listening: juvenile allocation shifts in response to acoustic cues of the social environment.

The social environment has a strong effect on the strength and direction of sexual selection. Juveniles, however, often have social cues that signal the current competitive environment which may provide cues of future competitive challenges. Here we demonstrate that juvenile crickets (Teleogryllus commodus) use the calls of surrounding adult males as a cue of the quality and density of rivals/mates they are likely to encounter. We reared hatchling crickets in six acoustic environments that varied in the density and quality of calls and demonstrate that individuals modified their development rate, phenotype and behaviour at maturity. Males matured more rapidly at a smaller size and called more when reared in a low competition environment. In contrast, males delayed maturity to grow larger when faced with an increased density of high‐quality males. Females matured more rapidly when reared in a high density of high‐quality males and allocated proportionately more resources towards egg production. A second experiment limiting nutrient availability demonstrates sex‐specific allocation shifts in the last stadium when cues are most reliable. Our results demonstrate that the social environment significantly affects allocation strategies and phenotypes, highlighting the importance of juvenile experience and competitive context when examining fitness and selection.

RECENT SOCIAL HISTORY ALTERS MALE COURTSHIP PREFERENCES

Phenotypically plastic mating behavior may allow males to modify their reproductive behavior to suit the prevailing social conditions, but we do not know if males only react to immediate social stimuli or change their inherent mate preferences according to their social history. Here we examine the effect of social experiences on the subsequent reproductive behavior of male guppies under standard conditions, allowing us to distinguish the effect of past and immediate social conditions. Males experienced experimental conditioning periods during which they interacted with three females, either of variable size or of similar size. Females arrived either simultaneously or consecutively. In subsequent standard assays, only males that had experienced females of variable size preferentially courted large females. Further, males exposed to sequential female arrival courted subsequent females more vigorously than males that had experienced simultaneous female arrival. In contrast, males did not alter their coercive mating attempts in relation to their recent social history. These results demonstrate that males use past experiences to modify their subsequent reproductive behavior rather than reacting only to immediate stimuli, and reveal the sophisticated ways in which males alter their reproductive tactics to suit the social environment and maximize fitness across changing selective landscapes.

Negative frequency-dependent preferences and variation in male facial hair

Negative frequency-dependent sexual selection maintains striking polymorphisms in secondary sexual traits in several animal species. Here, we test whether frequency of beardedness modulates perceived attractiveness of mens facial hair, a secondary sexual trait subject to considerable cultural variation. We first showed participants a suite of faces, within which we manipulated the frequency of beard thicknesses and then measured preferences for four standard levels of beardedness. Women and men judged heavy stubble and full beards more attractive when presented in treatments where beards were rare than when they were common, with intermediate preferences when intermediate frequencies of beardedness were presented. Likewise, clean-shaven faces were least attractive when clean-shaven faces were most common and more attractive when rare. This pattern in preferences is consistent with negative frequency-dependent selection.

Diversification of the eutherian placenta is associated with changes in the pace of life

Few mammalian organs vary as dramatically among species as the placenta. This variation is remarkable considering that the placenta’s primary function—transfer of nutrients and waste between mother and offspring—does not differ among species. Evolutionary changes in placental morphology remain poorly understood, with suggestions that parent–offspring conflict or evolutionary changes in life history might drive placental evolution. Here we demonstrate that life history differences among eutherian mammals are associated with major transitions in maternofetal interdigitation and placental invasiveness. We show that the repeated evolution of villous interdigitation is associated with reduced offspring production early in life and an increased lifespan. Further changes in placental morphology that reestablish a larger surface area are also associated with a change back to greater offspring production. After controlling for these differences in interdigitation, we also show that the least invasive placental type is associated with a fast pace of life. We predict that selection for a faster pace of life intensifies parent–offspring conflict, and that the repeated evolution of less-invasive placental structures might have allowed mothers to wrest back control of gestation from the fetus and alter their relative allocation to offspring production across life.

The effects of familiarity and group size on mating preferences in the guppy, Poecilia reticulata

Abstract In recent years, it has become evident that frequency dependence in the attractiveness of a particular phenotype to mates can contribute to the maintenance of polymorphism. However, these preferences for rare and unfamiliar male phenotypes have only been demonstrated in small, controlled experiments. Here, we tested the preference for unfamiliar mates in groups of six to 96 individuals over 13 days, in the guppy (Poecilia reticulata). We observed individual behaviour in situ to test whether fish discriminate two unfamiliar individuals among many familiar ones. We found that unfamiliar males and females were preferred over the familiar fishes in all groups and that this effect decayed over time. Increasing group sizes and levels of sexual activity did not hamper the preference for unfamiliar mates, providing further support for the role of frequency dependent mate choice in the maintenance of trait polymorphism in natural populations.

Selective Enrichment and Sequencing of Whole Mitochondrial Genomes in the Presence of Nuclear Encoded Mitochondrial Pseudogenes (Numts)

Numts are an integral component of many eukaryote genomes offering a snapshot of the evolutionary process that led from the incorporation of an α-proteobacterium into a larger eukaryotic cell some 1.8 billion years ago. Although numt sequence can be harnessed as molecular marker, these sequences often remain unidentified and are mistaken for genuine mtDNA leading to erroneous interpretation of mtDNA data sets. It is therefore indispensable that during the process of amplifying and sequencing mitochondrial genes, preventive measures are taken to ensure the exclusion of numts to guarantee the recovery of genuine mtDNA. This applies to mtDNA analyses in general but especially to studies where mtDNAs are sequenced de novo as the launch pad for subsequent mtDNA-based research. By using a combination of dilution series and nested rolling circle amplification (RCA), we present a novel strategy to selectively amplify mtDNA and exclude the amplification of numt sequence. We have successfully applied this strategy to de novo sequence the mtDNA of the Black Field Cricket Teleogryllus commodus, a species known to contain numts. Aligning our assembled sequence to the reference genome of Teleogryllus emma (GenBank EU557269.1) led to the identification of a numt sequence in the reference sequence. This unexpected result further highlights the need of a reliable and accessible strategy to eliminate this source of error.

Limited plasticity in the phenotypic variance‐covariance matrix for male advertisement calls in the black field cricket, Teleogryllus commodus

Phenotypic integration and plasticity are central to our understanding of how complex phenotypic traits evolve. Evolutionary change in complex quantitative traits can be predicted using the multivariate breeders’ equation, but such predictions are only accurate if the matrices involved are stable over evolutionary time. Recent study, however, suggests that these matrices are temporally plastic, spatially variable and themselves evolvable. The data available on phenotypic variance‐covariance matrix (P) stability are sparse, and largely focused on morphological traits. Here, we compared P for the structure of the complex sexual advertisement call of six divergent allopatric populations of the Australian black field cricket, Teleogryllus commodus. We measured a subset of calls from wild‐caught crickets from each of the populations and then a second subset after rearing crickets under common‐garden conditions for three generations. In a second experiment, crickets from each population were reared in the laboratory on high‐ and low‐nutrient diets and their calls recorded. In both experiments, we estimated P for call traits and used multiple methods to compare them statistically (Flury hierarchy, geometric subspace comparisons and random skewers). Despite considerable variation in means and variances of individual call traits, the structure of P was largely conserved among populations, across generations and between our rearing diets. Our finding that P remains largely stable, among populations and between environmental conditions, suggests that selection has preserved the structure of call traits in order that they can function as an integrated unit.