Kate Clancy, PhD

Wednesday, April 18th 2012

Your Ability to Handle Your Environment is Correlated with your Hormones

Natural selection acts not on a behavior itself, but on the factors that produce that behavior, and/or the outcome of that behavior. So if we want to have an evolutionary explanation for a behavior, it’s important to understand both what drives it and its consequences. We also need evidence that this behavior (or again, what comes before or after it) has some clear fitness benefit.

The kinds of factors that produce variation in behavior include things like resource availability, group composition, and mating strategies. How much food does the individual have access to, but also what kind? What do they need to do to acquire it and do they need to compete to do so? Who else is in the group and are they related to her? Is she a seasonal breeder or spontaneous ovulator, a promiscuous, monogamous, or polygynous primate?

So there are certainly good reasons to expect many behaviors to have adaptive significance, and for them to improve reproductive success. Yet when it comes to studying humans, too often this evolutionary buttressing collapses, only to be replaced with pop evolution interpretations. These interpretations tend to forget that things we find sexy today may or may not have been preferred in ancestral environments, and that if we cannot understand relationships between behavior and reproductive success without some sort of mechanism, it is little more than storytelling.

Hormones are one surefire way to begin to build a mechanistic link between behavior and reproductive success. Yet I am usually rather ornery about those manuscripts as well. When I complain about articles about hormones and behavior, they usually are based on the following issues:

So it’s nice to come across a paper* on hormones and behavior that not only manages not to fall into any of the above traps, but surpasses my expectations in terms of the quality of hypothesis testing, statistical analyses, and conclusions.

What they found
Ziomkiewicz et al (2012) found that urban, Polish women with a particular temperament profile – those with high activity and endurance traits but low emotional reactivity – had higher estradiol concentrations and a progesterone profile that rose earlier in the luteal phase compared to women with the opposite profile (low activity and endurance, high reactivity). They used the Formal Characteristics of Behavior – Temperament Inventory developed by Strelau and Zawadzki, and focused on activity, endurance and emotional reactivity because they correlate with personalities that indicate high reproductive success. In their supplementary materials, Ziomkiewicz et al more clearly define these traits:

Therefore women with high activity and endurance, but low emotional reactivity – and thus are emotionally stable and extraverted – are called High Ability to Process Stimulation (HAPS) individuals. Those with low activity and endurance but high emotional reactivity – so neurotic and introverted – are called Low Ability to Process Stimulation (LAPS) individuals.

The participants of this study were healthy, urban women from Wrocław, Poland, and they collected urine daily for one menstrual cycle. While there were 116 total participants, the main analyses of the paper compare HAPS and LAPS women, of which there were 26 participants each. This is still a great sample size for a study that has so much analytical richness per participant – for comparison, my own dissertation has half the number of participants (n = 25), and my only other major dataset 46 participants.

Behavior is context-dependent
Ziomkiewicz et al took a life history perspective on the question of whether ovarian hormones play a role in women’s personality. Women who are better at processing stimuli probably have more resources available to them, which makes them better equipped to handle the high resource demands of pregnancy, lactation and childcare. Women who are better at processing stimuli in their environment tend to be more extroverted and sociable, and extraversion and sociability are both highly preferred traits in potential mates, as well as correlated with reproductive success.

So, the authors hypothesized that HAPS women would have hormone profiles that indicate higher fertility compared to LAPS women. This is a far more thoughtful way to develop hypotheses about behavior and ovarian hormones because it comes from a basic principle of understanding that behavior is dependent on context and resource availability. That is, behavior is influenced by underlying genetic variation, and also environmental variation.

Ultimately, what Ziomkiewicz et al are arguing is that the mechanisms that underlie the relationship between extraversion and reproductive success reflect a relationship between these more basic temperamental traits of how well one handles one’s environment and ovarian hormones. So they are developing a model for how behavior is correlated with ovarian hormones in a way that is functionally, biologically significant. I think this is really cool!

Within a given population, if you have higher estradiol concentrations than the norm, you likely are able to allocate more energy both to ovulating a high-quality egg and getting your endometrium to grow nice and thick. If you also have high progesterone concentrations, it means you have a nice, big corpus luteum (that’s the yellow body left behind by the ovulated egg, again indicating it was probably high quality). Further, high progesterone indicates you can not only decidualize your endometrium, which means give it all the nooks and crannies and growth factors that make it a nice place to implant, but you can maintain the endometrium and a potential trophoblast until the placenta can make its own progesterone. This increases the chance for implantation and pregnancy but may also reduce the risk of early pregnancy loss.

The reason I make the point that all of this matters in terms of intrapopulation variation, is that different lifestyles and subsistence behaviors help produce populational norms for hormone concentrations. What is high for a rural Polish woman, for instance, is not the same as high for an urban Polish woman, and is probably not the same as high for an urban American woman. Not only that, but since these behaviors are context and resource-dependent, then the contexts and resources available to a given population, and how much they vary based on socioeconomic status and many other factors, are also important.

Physiology is context-dependent
This paper is cool for behavior people, but it’s also cool for reproductive physiology nerds like me. I mean, look at these graphs!

Profiles of urinary estrogen (a) and progesterone (b) during the menstrual cycle in HAPS (black circle) and LAPS (white square) women.

These are very likely biologically significant differences, at least in the estradiol curves. The authors did find that the day dependency of progesterone was different in the two groups, and you can see that while the overall values aren’t that different, that the HAPS women have higher values in the early part of the luteal phase. I would like to see these values aligned by ovulation so we can better see them up against the implantation window, which is 6-12 days after ovulation. Aligning there rather than menses might give us some better insight into whether this difference is biologically meaningful. If progesterone is higher in HAPS women in the early part of the window, that would definitely be interesting. And of course, it would be interesting to one day also run these analyses alongside other physiological variables like follicle waves or endometrial thickness.

Meeting the criteria for a good behavior paper
As I mentioned before, the following issues make me cranky:

Ziomkiewicz et al sampled daily throughout the menstrual cycle, provided a clear and coherent mechanistic link between hormones and behavior, and provided an interesting life history perspective on why temperament and ovarian hormones would be linked. The only criterion they don’t quite meet is in the use of an urban, Polish population, yet I still think this is different enough from the American and UK populations that are more often sampled that they pass here as well. From having done fieldwork in Poland over three summers, the activity patterns and diet composition is still pretty different in urban areas there versus in the US.

One final issue that Ziomkiewicz et al handle well is in discussing limitations and alternative hypotheses. They mention that energy availability can impact temperament, and so the relationship they found between temperament and ovarian hormones might only be the association between energy availability and ovarian hormones that has already been found countless times. However, they controlled for body fat, which partially addresses energy availability and the authors have previously shown influences estradiol.

From Ziomkiewicz et al 2008. Women with very low and high body fat have lower estradiol in this sample.

From Jasienska and Ellison 1998, demonstrating that higher energy expenditure is correlated with lower progesterone concentrations in this sample of rural, Polish women.

At the same time, differences in energy availability using other measures like energy expenditure and intake tend to affect progesterone and luteal activity first, as you can see in the figure above, yet that was definitely the lesser finding in this study. So I really think the authors have something here.

Of course I am biased (remember to see*), but I do think Ziomkiewicz and colleagues have put together a thoughtful and important contribution to our understanding of the ways in which behavior and hormones influence each other.

*Full disclosure: I know several of the authors on this paper and two (Ziomkiewicz and Jasienska) are collaborators. However I knew nothing of this project or manuscript until I saw the final, published form.

References
Jasienska G, Ellison PT. 1998. Physical work causes suppression of ovarian function in women. Proceedings of the Royal Society of London Series B 265(1408):1847-1851.

Ziomkiewicz A, Ellison PT, Lipson SF, Thune I, Jasienska G. 2008. Body fat, energy balance and estradiol levels: a study based on hormonal profiles from complete menstrual cycles. Hum Reprod 23(11):2555-2563.

Ziomkiewicz A, Wichary S, Bochenek D, Pawlowski B, Jasienska G. 2012. Temperament and ovarian reproductive hormones in women: Evidence from a study during the entire menstrual cycle. Hormones and Behavior 61(4):535-540.

Monday, April 9th 2012

American Association of Physical Anthropology Meetings this week: Portland, Oregon

Another year, another podium presentation. This year I want to redeem myself: last year I rocked my first presentation on hormonal contraception (woo hoo!), then was too exhausted to be remotely coherent for my second on diet composition and C-reactive protein (though to be fair, I was also chairing that session). This year I have just one presentation, which will allow me to concentrate on my talk, but also enjoy the meetings more.

A few highlights from the AAPAs this year include:

• A Building Babies get-together on Wednesday night (look for Julienne Rutherford and some obvious signage at the reception that evening)
• A Physical Anthropology Women’s Mentoring Network Happy Hour Thursday at 5:15pm in the Alexander’s Room on the 23rd floor of the Hilton
• A Biological Anthropology Developing Investigators Troop Happy Hour from 6-7pm on Friday, also in the Alexander’s Room on the 23rd floor of the Hilton.

So if you were involved with our book, are looking to give or receive some lady mentoring, and/or are a junior bio anthro colleague, there are chances for you to meet up with others.

Then there are, you know, the talks. The stuff you do between the schmoozing and the drinking. The Building Babies Lady Editors are all in the same, late Friday session (Session 24 in the Galleria North, 2-6pm). Guess who has the 5:45 talk?

This girl.

The relationship between strenuous physical activity and C-reactive protein is cycle-phase dependent: results from rural Poland

Energetic and inflammatory variables impact ovarian functioning, but their mechanistic links to each other and the ovaries remain unclear. We hypothesize that inflammatory biomarker C-reactive protein (CRP) is negatively correlated with strenuous physical activity in a population of rural Polish women. Because progesterone is suppressed by physical activity, yet progesterone administration can increase physical activity, we further hypothesized that their activity patterns would vary between the follicular and luteal phases, periods of low and high progesterone. Using standard epidemiological methods to collect daily records of minutes and exertion of physical activity over one menstrual cycle, we distinguished between light and strenuous activity, and activity variation through the cycle. Saliva was collected daily (progesterone), and urine seven times over the cycle (CRP).

Midluteal progesterone concentrations were inversely correlated with luteal CRP (p = 0.02), median CRP (p = 0.05), and were positively associated with strenuous activity in the luteal phase (p = 0.09). Median, luteal and follicular CRP were all negatively correlated with strenuous activity in the luteal phase (p = 0.03 for all three measures). And when women were grouped into those with high and low CRP concentrations, those with low CRP performed significantly more strenuous physical activity through the luteal phase. None of these associations were found with follicular phase physical activity. These results suggest physical activity influences systemic inflammation, which may additionally influence ovarian functioning. Therefore continued attention on systemic inflammation is crucial to determine mechanistic links between it and reproductive success in women.

Since writing this abstract my thinking on the topic has matured a bit (this is part of the problem with having an abstract deadline in September for a conference in April). We’ve also played around with the data a bit more, and have some more to report. I hope my presentation will get us thinking about subsistence versus recreational physical activity, as well as variation in strenuousness. I expect some of this will turn out to be pretty relevant to variation in reproductive function.

Friday, March 30th 2012

Building Babies: Interview with Julienne Rutherford

As I mentioned Wednesday, Building Babies, the volume edited by me, Katie Hinde and Julienne Rutherford will be out in only a few months in one of the fastest turnarounds I know of for a book of this nature. It also happens to be awesome.

I shared an interview with Lady Editor Katie on Wednesday, and today I share one with Lady Editor Julienne to describe how we developed this book, and why books like this are still important in academia (even if we could and should discuss issues in cost structures and accessibility). I also have printed the second half of the Building Babies table of contents, so that you can see the breadth of topics covered and our excellent chapter authors.

Building Babies Table of Contents (Part 2)

IV. MOTHERS AND INFANTS: THE FIRST SOCIAL RELATIONSHIP

12. Maternal influences on social and neural development in rhesus monkeys: Christopher J. Machado

13. Maternal Condition: Infant Compensation, Resilience, and Adaptive Response: Lynn A. Fairbanks and Katie Hinde

14. Tentative title: The role of mothers in the development of complex skills in chimpanzees: Elizabeth V. Lonsdorf

V. THE EXPANDING SOCIAL NETWORK

15. Reproductive Strategies and Infant Care in the Malagasy Primates: Stacey R. Tecot, Andrea L. Baden, Natalie Romine, Jason M. Kamilar

16. When dads help: infant development of owl monkeys and other primates with allo-maternal care: Maren Huck & Eduardo Fernandez Duque

17. Ontogeny of Social Behavior in the Genus Cebus and the Application of an Integrative Framework for Examining Plasticity and Complexity in Evolution: Katherine C. MacKinnon

VI. TRANSITIONS TO JUVENILITY AND REPRODUCTIVE MATURITY

18. Identifying proximate and ultimate causation in the development of primate sex-typed social behavior: Stephanie Meredith

19. Future adults or old children? Integrating life-history frameworks for understanding primate locomotor patterns: Michelle Bezanson and Mary Ellen Morbeck

20. Quantitative genetic perspectives female macaque life histories: heritability, plasticity, and trade-offs: Gregory Blomquist

21. Cultural evolution and human reproductive behavior: Lesley Newson

CONCLUSION (Robert Martin)

Interview with Julienne Rutherford, PhD, Assistant Professor, Department of Oral Biology, College of Dentistry, University of Illinois, Chicago

Julienne Rutherford hard at work, doing awesome science.

What was the experience like editing this book?
I had never done anything like this. I’ve done some co-writing and I’ve reviewed papers before, but the teamwork and choreography that go into an edited volume took those skills to a new level. I think it’s hilarious that Katie thought maybe I’d be smart enough to say no to editing a book as an as-yet untenured assistant professor. HAHAHAhahahaha. Um, no. But I have to say that even though I was warned and even strongly advised against doing this, it has turned out to be a real joy and so far one of my proudest professional achievements. I learned so much about editing (cutting extraneous prose, cleaning up narratives, tightening arguments, retaining an author’s voice through it all) and this in turn has already had a really positive impact on my own writing. And ultimately, it was just so fun to work with you and Katie and our incredibly talented cast of contributors.

What were some of the reasons you chose these chapter authors?
Their science is good, you know? We were just super jazzed about what is happening right now in the complex world of primate development. That said, I don’t want to shy away from the fact that it was very important to me personally to highlight new avenues of research into primate development being defined and pursued by junior scholars in our field, and especially women. We certainly did not include or exclude anyone just because of their gender – it really just turned out that the work we were most drawn to as exciting, interdisciplinary, innovative, and visionary was being done predominantly female scholars early in their careers. And I think that’s great.  If we can inspire each other, support each other’s scholarship, and really stand up for an inclusive intellectual culture, I hope our book makes a contribution to keeping women in the pipeline.

What is the value of an edited volume in this era of academic publishing?
The value to me is that it allowed us to craft a specific kind of narrative in a specific time in the history of the field of primate development. The chapters bring to the forefront complementary themes like epigenetics and evo-devo, inflammation and stress, developmental transitions.  Certainly some of the avenues outlined in the book are in their infancy – hee, I made a Building Babies pun! – and we will see how they bear out over time. But an edited volume is sort of like staking a flag, a grand gesture because we are saying that this is for posterity, in a way that a special journal issue or meeting proceedings doesn’t achieve, in my view. I also want to point out that our review process was unusually rigorous for an edited volume (I’m sure many of our contributors would agree with that!) but that meant that everyone really had to make a concerted effort to be intelligible to each other. So the book in many ways forms a conversation, a really nerdtastic conversation.

What contribution do you think this book makes to anthropology? To evolutionary biology?
We take an explicitly comparative approach to primate development. By that I mean that we don’t divide this book along taxonomic lines. Since our organizing frame is the developmental trajectory, we are talking about humans, baboons, lemurs, chimpanzees, et cetera, all in the same breath. I think it’s enormously important that the study of human biology and human biomedicine is integrated into a comparative primatology. I can’t help find it odd that we train human biologists in some anthropology programs with nothing but the barest bones of a primatology background. Many human biologists are really well-versed in the rodent literature that pertains to their particular phenomena of interest, and are really well-versed in human physiology, but are not aware of the amazing work their primatological colleagues are doing. I anticipate this book helping to foster a cross-pollination that I think will be tremendously beneficial to the future of biological anthropology. See, I have a dream of a world in which a biological anthropologist who works on both human and nonhuman primate projects makes sense to hiring committees and funding agencies, and if that’s wrong, I don’t want to be right.