Balancing Act: an Interdisciplinary Exploration of Trade-offs in Reproducing Females.

Trade-offs resulting from the high demand of offspring production are a central focus of many subdisciplines within the field of biology. Yet, despite the historical and current interest on this topic, large gaps in our understanding of whole-organism trade-offs that occur in reproducing individuals remain, particularly as it relates to the nuances associated with female reproduction. This volume of Integrative and Comparative Biology (ICB) contains a series of papers that focus on reviewing trade-offs from the female-centered perspective of biology (i.e., a perspective that places female reproductive biology at the center of the topic being investigated or discussed). These papers represent some of the work showcased during our symposium held at the 2024 meeting of the Society for Integrative and Comparative Biology (SICB) in Seattle, Washington. In this roundtable discussion, we use a question-and-answer format to capture the diverse perspectives and voices involved in our symposium. We hope that the dialogue featured in this discussion will be used to motivate researchers interested in understanding trade-offs in reproducing females and provide guidance on future research endeavors.

Let's talk about sex: instructor views and hesitancies related to sex and gender in the biology classroom.

There is much current debate in the US regarding how sex and gender are approached in science and medical classrooms. There does not seem to be sufficient consensus around why it must be taught and how it should be implemented. State-enacted restrictions to both education and healthcare in recent years demonstrate the relevance and importance of sex and gender in the college classroom, not only including but especially in the biology classroom. Given the areas comprising the Society for Integrative and Comparative Biology (SICB), these topics of sex and gender in biology instruction are incredibly salient to our members. Thus, this survey aimed to determine instructors' views of and experiences with sex-diverse gender-inclusive biology. College-level biology instructors who are members of SICB were surveyed about their views of science, views of sex and gender, teaching philosophy, and their experiences with inclusive teaching and with sex-diverse gender-inclusive teaching. The resulting data lead us to implore academic biology to provide more sex-diverse and gender-inclusive teaching tools and resources to educators, while minimizing potential fear of retaliation and backlash to instructors who utilize these teaching methods.

Incorporating Sex-Diverse and Gender-Inclusive Perspectives in Higher Education Biology Courses.

Inclusive teaching is teaching in a way that reaches all students in the classroom; this is beneficial for everyone and particularly for those with minoritized identities. Instructors play a critical role in scaffolding how students are exposed to and learn science content in the classroom. In this manuscript we discuss how biology instructors can make their classrooms more inclusive with regard to sex and gender diversity content. Many topics in biology are based on androcentric, heteronormative, and oppressive framing, even though those lenses are more reflective of our own history and culture than they are of the diversity we see in nature. Here, we summarize information presented in the SICB 2024 workshop titled "Incorporating sex diversity and gender inclusivity in biology undergraduate classrooms" and provide instructors with a) rationale for why inclusive teaching matters, b) guidance on how to challenge unscientific views and make their curricula more sex-diverse and gender inclusive, and c) practical and easy-to-implement strategies for discussing "contentious" topics in the classroom. Incorporation of this material will be beneficial for students, for science and medicine, and for accurately representing the diversity found across the tree of life.

Understanding Patterns of Life History Trait Covariation in an Untapped Resource, the Lab Mouse.

AbstractThrough artificial selection and inbreeding, strains of laboratory mice have been developed that vary in the expression of a single or suite of desired traits valuable to biomedical research. In addition to the selected trait(s), these strains also display variation in pelage color, body size, physiology, and life history. This article exploits the broad phenotypic variation across lab mouse strains to evaluate the relationships between life history and metabolism. Life history variation tends to exist along a fast-slow continuum. There has been considerable interest in understanding the ecological and evolutionary factors underlying life history variation and the physiological and metabolic processes that support them. Yet it remains unclear how these key traits scale across hierarchical levels, as ambiguous empirical support has been garnered at the intraspecific level. Within-species investigations have been thwarted by methodological constraints and environmental factors that obscure the genetic architecture underlying the hypothesized functional integration of life history and metabolic traits. In this analysis, we used the publicly available Mouse Phenome Database by the Jackson Laboratory to investigate the relationships among life history traits (e.g., body size, reproduction, and life span) and metabolic traits (e.g., daily energy expenditure and insulin-like growth factor 1 concentration). Our findings revealed significant variation in reproductive characteristics across strains of mice as well as relationships among life history and metabolic traits. We found evidence of variation along the fast-slow life history continuum, though the direction of some relationships among these traits deviated from interspecific predictions laid out in previous literature. Furthermore, our results suggest that the strength of these relationships are strongest earlier in life.

Chronic Stress Decreases Lactation Performance.

The ability to provision offspring with milk is a significant adaptive feature of mammals that allows for considerable maternal regulation of offspring beyond gestation, as milk provides complete nutrition for developing neonates. For mothers, lactation is a period of marked increases in energetic and nutritive demands to support milk synthesis; because of this considerable increase in demand imposed on multiple physiological systems, lactation is particularly susceptible to the effects of chronic stress. Here, we present work that explores the impact of chronic stress during lactation on maternal lactation performance (i.e., milk quality and quantity) and the expression of key milk synthesis genes in mammary tissue using a Sprague-Dawley rat model. We induced chronic stress using a well-established, ethologically relevant novel male intruder paradigm for 10 consecutive days during the postpartum period. We hypothesized that the increased energetic burden of mounting a chronic stress response during lactation would decrease lactation performance. Specifically, we predicted that chronic exposure to this social stressor would decrease either milk quality (i.e., composition of proximate components and energy density) or quantity. We also predicted that changes in proximate composition (i.e., lipid, lactose, and protein concentrations) would be associated with changes in gene expression levels of milk synthesis genes. Our results supported our hypothesis that chronic stress impairs lactation performance. Relative to the controls, chronically stressed rats had lower milk yields. We also found that milk quality was decreased; milk from chronically stressed mothers had lower lipid concentration and lower energy density, though protein and lactose concentrations were not different between treatment groups. Although there was a change in proximate composition, chronic stress did not impact mammary gland expression of key milk synthesis genes. Together, this work demonstrates that exposure to a chronic stressor impacts lactation performance, which in turn has the potential to impact offspring development via maternal effects.

Why Students Struggle in Undergraduate Biology: Sources and Solutions.

Students' perceptions of challenges in biology influence performance outcomes, experiences, and persistence in science. Identifying sources of student struggle can assist efforts to support students as they overcome challenges in their undergraduate educations. In this study, we characterized student experiences of struggle by 1) quantifying which external factors relate to perceptions of encountering and overcoming struggle in introductory biology and 2) identifying factors to which students attribute their struggle in biology. We found a significant effect of Course, Instructor, and Incoming Preparation on student struggle, in which students with lower Incoming Preparation were more likely to report struggle and the inability to overcome struggle. We also observed significant differences in performance outcomes between students who did and did not encounter struggle and between students who did and did not overcome their struggle. Using inductive coding, we categorized student responses outlining causes of struggle, and using axial coding, we further categorized these as internally or externally attributed factors. External sources (i.e., Prior Biology, COVID-19, External Resources, Classroom Factors) were more commonly cited as the reason(s) students did or did not struggle. We conclude with recommendations for instructors, highlighting equitable teaching strategies and practices.

Why Did Students Report Lower Test Anxiety during the COVID-19 Pandemic?

Test anxiety is a common experience shared by college students and is typically investigated in the context of traditional, face-to-face courses. However, the onset of the COVID-19 pandemic resulted in the closure of universities, and many students had to rapidly shift to and balance the challenges of online learning. We investigated how the shift to online learning during the pandemic impacted trait (habitual) and state (momentary) test anxiety and whether there was variation across different demographic groups already vulnerable to performance gaps in science, technology, engineering, and mathematics (STEM) courses. Quantitative analyses revealed that trait and state test anxiety were lower in Spring 2020 (COVID semester) than in Spring 2019 and were higher overall in women than men. We did not find a difference in either trait or state anxiety in first-generation students or among persons excluded because of ethnicity or race. Qualitative analyses revealed that student priorities shifted away from coursework during Spring 2020. While students initially perceived the shift to online learning as beneficial, 1 month after the shift, students reported more difficulties studying and completing their coursework. Taken together, these results are the first to compare reports of test anxiety during a traditional, undisrupted semester to the semester where COVID-19 forced a sudden transition online.

Changes in maternal fecal corticosterone metabolites across lactation and in response to chronic stress.

Maternal exposure to stressors during lactation has previously been demonstrated to impact various aspects of milk synthesis and to have long-term physiological effects on offspring. Much of the current literature investigating the effects of stress during lactation has used acute stressors, and the studies investigating the effects of chronic stressors largely focus on neurological changes. Further, temporal variation in glucocorticoids across lactation in response to stressors has rarely been assessed. The present work uses a novel male intruder paradigm to model the effects of chronic stress on maternal fecal corticosterone metabolites (FCMs) in Sprague-Dawley rats across lactation. FCM levels were elevated in chronically-stressed mothers relative to the control group. Further, FCMs in the stress group were time-dependent either due to repeated exposure to the stressor or lactation stage. Together, this work demonstrates the efficacy of this established paradigm in increasing circulating glucocorticoids in lactating rats. These results highlight the need for repeated temporal sampling, as glucocorticoid levels in response to a chronic stressor may change across lactation.

Methodological Considerations for Assessing Immune Defense in Reproductive Females.

One of the key foci of ecoimmunology is understanding the physiological interactions between reproduction and immune defense. To assess an immune challenge, investigators typically measure an immune response at a predetermined time point that was selected to represent a peak response. These time points often are based on the immunological responses of nonreproductive males. Problematically, these peaks have been applied to studies quantifying immune responses of females during reproduction, despite the fact that nonreproductive males and reproductive females display fundamentally different patterns of energy expenditure. Previous work within pharmacological research has reported that the response to the commonly-used antigen keyhole limpet hemocyanin (KLH) varies among individuals and between females and males. In this heuristic analysis, we characterize antibody responses to KLH in females with varying reproductive demands (nonreproductive, lactating, concurrently lactating, and pregnant). Serum was taken from one animal per day per group and assessed for general and specific Immunoglobulins (Igs) G and M. We then used regression analysis to characterize the antibody response curves across groups. Our results demonstrate that the antibody response curve is asynchronous among females with varying maternal demands and temporally differs from the anticipated peak responses reflected in standardized protocols. These findings highlight the importance of multiple sampling points across treatment groups for a more integrative assessment of how reproductive demand alters antibody responses in females beyond a single measurement.

It Takes Two to Tango: Including a Female Perspective in Reproductive Biology.

Like many scientific disciplines, the field of reproductive biology is subject to biases in terminology and research foci. For example, females are often described as coy and passive players in reproductive behaviors and are termed "promiscuous" if they engage in extra-pair copulations. Males on the other hand are viewed as actively holding territories and fighting with other males. Males are termed "multiply mating" if they mate with multiple females. Similarly, textbooks often illustrate meiosis as it occurs in males but not females. This edition of Integrative and Comparative Biology (ICB) includes a series of papers that focus on reproduction from the female perspective. These papers represent a subset of the work presented in our symposium and complementary sessions on female reproductive biology. In this round table discussion, we use a question and answer format to leverage the diverse perspectives and voices involved with the symposium in an exploration of theoretical, cultural, pedagogical, and scientific issues related to the study of female biology. We hope this dialog will provide a stepping-stone toward moving reproductive science and teaching to a more inclusive and objective framework.

Social Interaction With an Alcohol-Intoxicated or Cocaine-Injected Peer Selectively Alters Social Behaviors and Drinking in Adolescent Male and Female Rats.

BACKGROUND: Drinking alcohol is facilitated by social interactions with peers, especially during adolescence. The importance of peer social influences during adolescence on alcohol and substance use has recently received more attention. We have shown that social interaction with an alcohol-intoxicated peer influences adolescent alcohol drinking differently in male and female rats using the demonstrator-observer paradigm. The present set of experiments analyzed the social interaction session to determine changes in social behaviors and subsequent alcohol drinking in adolescent male and female rats. METHODS: Specifically, in Experiment 1, we determined whether specific social behaviors were altered during interaction with an alcohol-intoxicated demonstrator administered 1.5 g/kg ethanol (EtOH) and assessed changes in EtOH intake in adolescent observers. Experiment 2 examined changes in voluntary saccharin consumption to determine whether social interaction with an alcohol-intoxicated demonstrator administered 1.5 g/kg EtOH altered consumption of a palatable solution. In Experiment 3, we administered saline, and a low (5 mg/kg) or high (20 mg/kg) dose of cocaine to the demonstrator and assessed changes in the adolescent observers to determine whether social interaction with a "drugged" peer altered social behaviors and voluntary EtOH intake. RESULTS: We showed that social interaction with an alcohol-intoxicated demonstrator administered 1.5 g/kg EtOH (i) decreased social play and increased social investigation and social contact in adolescent male and female observers, (ii) did not alter nonsocial behaviors, (iii) did not alter saccharin consumption, and (iv) increased voluntary EtOH intake in adolescent female but not male observers. When the peer was injected with cocaine, (i) social play was dose-dependently decreased, (ii) there were no changes in other social or nonsocial behaviors, and (iii) voluntary EtOH intake in adolescent male and female observers was unaffected. CONCLUSIONS: The present results are consistent and extend our previous work, showing that social interaction with an alcohol-intoxicated peer selectively alters social behaviors and alcohol drinking in adolescent rats. Females appear to be more sensitive to the elevating effects of social interaction on voluntary EtOH consumption.

Bacterial Pathogen Emergence Requires More than Direct Contact with a Novel Passerine Host.

While direct contact may sometimes be sufficient to allow a pathogen to jump into a new host species, in other cases, fortuitously adaptive mutations that arise in the original donor host are also necessary. Viruses have been the focus of most host shift studies, so less is known about the importance of ecological versus evolutionary processes to successful bacterial host shifts. Here we tested whether direct contact with the novel host was sufficient to enable the mid-1990s jump of the bacterium Mycoplasma gallisepticum from domestic poultry to house finches (Haemorhous mexicanus). We experimentally inoculated house finches with two genetically distinct M. gallisepticum strains obtained either from poultry (Rlow) or from house finches (HF1995) during an epizootic outbreak. All 15 house finches inoculated with HF1995 became infected, whereas Rlow successfully infected 12 of 15 (80%) inoculated house finches. Comparisons among infected birds showed that, relative to HF1995, Rlow achieved substantially lower bacterial loads in the host respiratory mucosa and was cleared faster. Furthermore, Rlow-infected finches were less likely to develop clinical symptoms than HF1995-infected birds and, when they did, displayed milder conjunctivitis. The lower infection success of Rlow relative to HF1995 was not, however, due to a heightened host antibody response to Rlow. Taken together, our results indicate that contact between infected poultry and house finches was not, by itself, sufficient to explain the jump of M. gallisepticum to house finches. Instead, mutations arising in the original poultry host would have been necessary for successful pathogen emergence in the novel finch host.

Mitochondrial function, ornamentation, and immunocompetence.

Understanding the mechanisms that link ornamental displays and individual condition is key to understanding the evolution and function of ornaments. Immune function is an aspect of individual quality that is often associated with the expression of ornamentation, but a general explanation for why the expression of some ornaments seems to be consistently linked to immunocompetence remains elusive. We propose that condition-dependent ornaments may be linked to key aspects of immunocompetence through co-dependence on mitochondrial function. Mitochondrial involvement in immune function is rarely considered outside of the biomedical literature, but the role of mitochondria as the primary energy producers of the cell and the centres of biosynthesis, the oxidative stress response, and cellular signalling place them at the hub of a variety of immune pathways. A promising new mechanistic explanation for correlations between a wide range of ornamental traits and the properties of individual quality is that mitochondrial function may be the 'shared pathway' responsible for links between ornament production and individual condition. Herein, we first review the role of mitochondria as both signal transducers and metabolic regulators of immune function. We then describe connections between hormonal pathways and mitochondria, with implications for both immune function and the expression of ornamentation. Finally, we explore the possibility that ornament expression may link directly to mitochondrial function. Considering condition-dependent traits within the framework of mitochondrial function has the potential to unify central tenets within the study of sexual selection, eco-immunology, oxidative stress ecology, stress and reproductive hormone biology, and animal physiology.