Who listens to mother?:A whole-family perspective on the evolution of maternal hormone allocation

Maternal effects, or the influence of maternal environment and phenotype on offspring phenotype, may allow mothers to fine-tune their offspring's developmental trajectory and resulting phenotype sometimes long after the offspring has reached independence. However, maternal effects on offspring phenotype do not evolve in isolation, but rather within the context of a family unit, where the separate and often conflicting evolutionary interests of mothers, fathers and offspring are all at play. While intrafamilial conflicts are routinely invoked to explain other components of reproductive strategy, remarkably little is known about how intrafamilial conflicts influence maternal effects. We argue that much of the considerable variation in the relationship between maternally derived hormones, nutrients and other compounds and the resulting offspring phenotype might be explained by the presence of conflicting selection pressures on different family members. In this review, we examine the existing literature on maternal hormone allocation as a case study for maternal effects more broadly, and explore new hypotheses that arise when we consider current findings within a framework that explicitly incorporates the different evolutionary interests of the mother, her offspring and other family members. Specifically, we hypothesise that the relationship between maternal hormone allocation and offspring phenotype depends on a mother's ability to manipulate the signals she sends to offspring, the ability of family members to be plastic in their response to those signals and the capacity for the phenotypes and strategies of various family members to interact and influence one another on both behavioural and evolutionary timescales. We also provide suggestions for experimental, comparative and theoretical work that may be instrumental in testing these hypotheses. In particular, we highlight that manipulating the level of information available to different family members may reveal important insights into when and to what extent maternal hormones influence offspring development. We conclude that the evolution of maternal hormone allocation is likely to be shaped by the conflicting fitness optima of mothers, fathers and offspring, and that the outcome of this conflict depends on the relative balance of power between family members. Extending our hypotheses to incorporate interactions between family members, as well as more complex social groups and a wider range of taxa, may provide exciting new developments in the fields of endocrinology and maternal effects.</p

Introducing biological realism into the study of developmental plasticity in behaviour

There is increasing attention for integrating mechanistic and functional approaches to the study of (behavioural) development. As environments are mostly unstable, it is now often assumed that genetic parental information is in many cases not sufficient for offspring to become optimally adapted to the environment and that early environmental cues, either indirectly via the parents or from direct experience, are necessary to prepare them for a specific environment later in life. To study whether these early developmental processes are adaptive and through which mechanism, not only the early environmental cues but also how they impinge on the later-life environmental context has therefore to be taken into account when measuring the animal's performance. We first discuss at the conceptual level six ways in which interactions between influences of different time windows during development may act (consolidation, cumulative information gathering and priming, compensation, buffering, matching and mismatching, context dependent trait expression). In addition we discuss how different environmental factors during the same time window may interact in shaping the phenotype during development. Next we discuss the pros and cons of several experimental designs for testing these interaction effects, highlighting the necessity for full, reciprocal designs and the importance of adjusting the nature and time of manipulation to the animal's adaptive capacity. We then review support for the interaction effects from both theoretical models and animal experiments in different taxa. This demonstrates indeed the existence of interactions at multiple levels, including different environmental factors, different time windows and between generations. As a consequence, development is a life-long, environment-dependent process and therefore manipulating only the early environment without taking interaction effects with other and later environmental influences into account may lead to wrong conclusions and may also explain inconsistent results in the literature.</p

Male-Male Competition as a Force in Evolutionary Diversification: Evidence in Haplochromine Cichlid Fish

It has been suggested that intrasexual competition can be a source of negative frequency-dependent selection, causing agonistic character displacement and facilitating speciation and coexistence of (sibling) species. In this paper we synthesise the evidence that male-male and female-female competition contributes to cichlid diversification, showing that competition is stronger among same-coloured individuals than those with different colours. We argue that intrasexual selection is more complex because there are several examples where males do not bias aggression towards their own type. In addition, sibling species or colour morphs often show asymmetric dominance relationships. We briefly discuss potential mechanisms that might promote the maintenance of covariance between colour and aggression-related traits even in the face of gene-flow. We close by proposing several avenues for future studies that might shed more light on the role of intrasexual competition in cichlid diversification

High maternal androstenedione levels during pregnancy in a small precocial mammal with female genital masculinisation

-Masculinisation of female genitalia is an intriguing phenomenon amongst some mammalian species and its endocrinological basis as well as its adaptive value is still heavily debated. We recently reported female genital masculinisation in Cavia magna. The closely related C. aperea, does not show such masculinisation providing an unique opportunity to investigate potential endocrinological mechanisms underlying this difference. For both species we determined plasma levels of androstenedione and testosterone in adults of both sexes, and in females during different stages of pregnancy. Consistent with the normal mammalian pattern males showed higher levels of both androgens than conspecific females. Androgen profiles during pregnancy differed significantly between C. magna and C. aperea females: during mid-pregnancy androstenedione levels were strongly elevated in the masculinised C. magna, but not in C. aperea, indicating that high levels of this androgen may be involved in the differentiation of masculinized genitalia in female C. magna, as has been suggested for the spotted hyena. In both C. magna and the spotted hyena the pups show a highly advanced state of maturation, but in contrast to the hyena female C. magna are not overly aggressive. We therefore propose that female genital masculinisation might be a side effect of early exposure to elevated levels of maternal androgens that might be selected for to speed up precocial development.

The relationship between male social status, ejaculate and circulating testosterone concentration and female yolk androgen transfer in red junglefowl (<i>Gallus gallus</i>)

Several studies show that avian females prefer males based on their secondary sexual ornaments and dominance status. We tested in red junglefowl (Goth's gallus) how comb size affected the result of fighting and how the dominance status related to testosterone concentrations in their circulation and ejaculates. We subsequently tested how social status was related to female reproductive investment, including yolk hormone transfer. We found that after a fight 1) winners increased plasma T and decreased ejaculates T whereas losers' T remained unchanged, and 2) plasma T of winners was higher but ejaculates T was lower than those of losers. We argued those are consistent with the different reproductive strategies of dominant and subordinate males. Furthermore, in line with offspring sex-dependent growth patterns females transferred significantly more androstenedione to female than male embryos when mated with winners, while doing the opposite when mated with losers. We concluded therefore that female reproductive investment was affected by both partner quality and embryo sex. The results indicate that male quality influences sex-specific maternal investment, which could be mediated by ejaculate testosterone concentration

Interactions between prenatal maternal effects and posthatching conditions in a wild bird population

Resources and cues provided by the mother before birth are important mediators of developmental plasticity. It has been suggested that the adaptive value of such prenatal maternal effects may depend on the environment encountered by the offspring after birth, and that offspring may perform better when environmental conditions encountered by the mother and the offspring match, than when a mismatch occurs. Here, we test how prenatal maternal effects and postnatal conditions interact in influencing offspring growth and development in wild-living great tits (Parus major) by manipulating food availability experienced by the mother before egg laying, partially cross-fostering nestlings between nests, and manipulating food availability after hatching. We observed significant interaction effects between pre- and postnatal food conditions. Nonsupplemented nestlings reached a similar fledging mass, a trait closely linked to postfledging survival, as food-supplemented nestlings when their biological mother had received extra food during egg laying. It shows that prenatal maternal investment can compensate for growth-limiting conditions after hatching. This effect was sex specific, with daughters benefiting more than sons. Furthermore, food-supplemented nestlings grew largest when their biological mother had not received extra food during egg laying, suggesting that offspring were primed prenatally, possibly through differential egg composition, to use resources more efficiently. However, we found no evidence that offspring performed generally better when pre- and postnatal food conditions matched than when a mismatch occurred. Our results demonstrate the importance of considering the postnatal environment when testing for the ecological and evolutionary consequences of prenatal maternal effects in natural population

Differential maternal testosterone allocation among siblings benefits both mother and offspring in the Zebra finch <i>Taeniopygia guttata</i>

Parents are selected to preferentially invest in the offspring with highest reproductive value. One mechanism for achieving this is the modification of competitive asymmetries between siblings by maternal hormones. In many organisms, offspring value varies according to birth position in the brood, which determines survival chances and competitive advantage over access to resources. In birds, variation in yolk androgen allocation over the laying sequence is thought to modulate dominance of senior chicks over junior brood mates. We tested this hypothesis in zebra finches, which show a naturally decreasing pattern of within-clutch testosterone allocation. We abolished these within-clutch differences by experimentally elevating yolk testosterone levels in eggs 2-6 to the level of egg 1, and we assessed fitness measures for junior offspring (eggs 2-6), senior offspring (egg 1), and their mothers. Testosterone-injected eggs hatched later than control eggs. Junior, but not senior, chicks in testosterone-treated broods attained poorer phenotypic quality compared to control broods, which was not compensated for by positive effects on seniors. Mothers were generally unaffected by clutch treatment. Thus, naturally decreasing within-clutch yolk testosterone allocation appears to benefit all family members and does not generally enhance brood reduction by favoring senior chicks, in contrast to the widely held assumption

Differential survival between visual environments supports a role of divergent sensory drive in cichlid fish speciation

Identifying the selective forces that initiate ecological speciation is a major challenge in evolutionary biology. Sensory drive has been implicated in speciation in various taxa, largely based on phenotype-environment correlations and signatures of selection in sensory genes. Here, we present a reciprocal transplant experiment revealing species differences in performance in alternative visual environments, consistent with speciation by divergent sensory drive. The closely related cichlids Pundamilia pundamilia and Pundamilia nyererei inhabit different visual environments in Lake Victoria and show associated differences in visual system properties. Mimicking the two light environments in the laboratory, we find a substantial reduction in survival of both species when reared in the other species’ visual environment. This implies that the observed differences in Pundamilia color vision are indeed adaptive and substantiates the implicit assumption in sensory drive speciation models that divergent environmental selection is strong enough to drive divergence in sensory properties

Born to win?:Testing the fighting hypothesis in realistic fights: Left-handedness in the Ultimate Fighting Championship

Given the heritability of human left-handedness and its purported associations with fitness-lowering traits, the persistence of the minority of left-handedness in human populations is an evolutionary puzzle. The fighting hypothesis proposes that these negative fitness costs are offset by fitness gains for left-handers when involved in fights with right-handers, as being a minority would generate a surprise effect increasing the chance of winning. The finding that left-handers are overrepresented in many combat sports is interpreted as evidence for this hypothesis. However, few studies have examined sports that show good similarity with realistic fights and analysed winning chances in relation to handedness of both fighters. We examined both, in a sample of the Ultimate Fighting Championship (UFC), a fierce fighting sport hardly constrained by rules. Left-handers were strongly overrepresented as compared to the general male population but no advantage for left-handers when facing right-handers was found, providing only partial evidence for the fighting hypothesis. (C) 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.</p

The importance of understanding function and evolution

Ocklenburg et al. (2020, Laterality 2020: Entering the next decade. Laterality) provided the field of laterality research with a stimulating research perspective for the coming decade, based on the current state of the art in both animal and human laterality research. Although this is paper takes many different approaches of laterality into account, we emphasize that the eco-evolutionary approach needs more attention. This concerns the question why organisms are lateralized in the first place, in other words, how does lateralization enhance the Darwinian fitness of the individual. We argue that laterality can be distinguished along four dimensions, and that each of them requires different ultimate explanations. Studying these functional and evolutionary explanations requires the development of ecologically relevant tests, adapted to the species at hand. It also requires experimental manipulation of laterality, testing the effect in (semi)-natural conditions on fitness parameters. Tools for such manipulation of laterality urgently require a better understanding of the developmental plasticity of lateralization, extending the field of evo-devo to that of eco-evo-devo. We also warn against seeing the minority in the distribution of direction or strength of lateralization as being a pathology as such minorities in biology can often be explained as adaptations by natural frequency dependent selection