Are Life History Trade-Offs Based On Function?

Nicole Barbaro, Ph.D.
7 min readAug 1, 2019

A New Study [IN BUGS] Suggests Caution of Basic Theoretical Assumption

by Nicole Barbaro

When I get to my office in the morning, I go through my email and read my journal alerts of the newest academic papers published. I often come across papers that are interesting, but today I came across a paper that really blew me away. Why? Because it used a clever research design to yield big theoretical implications — my favorite kind of paper.

The paper, “A Weapons-Testes Trade-Off In Males Is Amplified in Female Traits,” by Christine Miller, Paul Joseph, Rebecca Kilner, and Zachary Emberts published in Proceedings B caught my attention. My lab recently published a paper on trade-offs in male ejaculate quality using a life history framework, so I was interested to see how the findings of this new paper contributed to this broader research area. The research did not disappoint. The results certainly found trade-offs between weapons and testes as the title implies, but with a significant twist, humbly reflected by the last part of the title “amplified in female traits.”

The paper published 31 July 2019 in Proceedings B.

Life history theory is a biological framework that attempts to explain fitness trade-offs between (and within) species. The notion of trade-offs centers around the fact that resources organisms use — time, energy — are finite, or limited. Because an organism only has so many resources available at any one time, the organism must make decisions (not necessarily consciously!) about the best investment of those resources to various life functions. There are some functional domains that are fundamental according to the theory: reproduction, growth, and survival. Given that reproduction is central to the evolution of sexually reproducing species, life history research across organisms largely focuses on reproductive trade-offs.

In most sexually reproducing species, there are two arenas of reproductive competition that are called pre-copulatory competition, or competition that occurs prior to sex (often times) between males for access to a mate; and post-copulatory competition, or competition that occurs after sex between sperm (often times) in the female reproductive tract.

These arenas of competition require different skill-sets. Pre-copulatory competition requires big weapons to dominate other males for access to females (think horns, muscle, or in the case of the current paper, big legs). Post-copulatory competition, however, requires quality sperm that can successfully navigate through the female reproductive tract to the coveted prize ovum. Because fertilization is a big numbers game (more sperm = better chances of fertilization), big testes, rather than big weapons, are most useful in the post-copulatory competitive arena.

Growing big weapons and big testes, however, are energetically expensive and require a lot of resources to produce. Thus, across and within species it is presumed that there is a trade-off between weapon production and testes size: energy devoted to weapon growth for pre-copulatory competition is energy that can’t be allocated to testes growth (and sperm production) for post-copulatory competition, and vice versa. This weapon-testes trade-off falls into the “reproduction” category of life history trade-offs. In other words, there is resource competition within the functional category of reproduction — allocate resources to get access to a mate or allocate resources to fertilize eggs.

So far, so good. Much of the research on pre- and post-copulatory competition and the associated trade-offs is done in non-humans, and particularly in bugs for a host of methodological and ethical reasons. Simply put, you can do experiments with bugs that you just can’t do with humans. Such as, chopping off legs to see if testes grow bigger as a result.

The research by Miller et al. did exactly that — chop off a male’s weapon and see whether testes grow bigger as a result. Resources allocated to weapon growth are significantly reduced, and therefore resources can be allocated to testes growth and sperm production. Exactly in line with assumed functional life history trade-offs.

Miller et al. chose leaf-footed cactus bugs (Narnia femorata) for the experiment. These bugs have a unique trait that made them a clever subject for this research: big, muscular hind-legs. Males and females both have enlarged hind-legs that aid in locomotion, but males also use them for a different purpose. Males use their hind-legs as weapons in male-male contests for mates (pre-copulatory competition), whereas females have never been observed using them in competition.

A leaf-footed cactus bug, the species used in the Miller et al. paper. Note the big hind-legs!

This sex-difference in use of these weapons offered a unique opportunity for Miller et al. to test if trade-offs between weapons and testes reflected a functional life history trade-off within the reproductive domain (pre- vs. post-copulatory competition) mentioned above, or if the weapon-testes trade-off reflected some other trade-off that is not due to the functional grouping of weapons and testes, such as the general expense of growing tissues, or developmental timing.

Because female cactus bugs also have enlarged hind-legs, like males, testing this hypothesis was possible. Female hind-legs have no role in reproduction, so if female gonad size increased as a result of removing a hind-leg, the same as what is expected in the males, then the result would suggest that life history trade-offs are not based on functional grouping as assumed by theory, but rather may reflect more general processes of, say, tissue expense, for example.

Miller et al. bred cactus bugs in the lab, and chopped off one of the hind-legs of male and female cactus bugs at an appropriate developmental stage previously validated by other experiments in this species (it is also apparently not uncommon for males and females to lose one of their hind-legs in the wild due to various reasons.) The group of autotomized (one-legged) cactus bugs were compared to a control group of in-tact cactus bugs on subsequent testis and ovary size in the males and females.

As expected, autotomized males grew larger testes, but did not grow larger overall, nor did their remaining hind-leg have greater muscle mass. What about the females? Females who had one of their hind-legs removed also grew larger ovaries with more oocytes. As with the males, autotomized females did not grow larger overall, nor did their remaining hind-leg have greater muscle mass. Also, the increase in ovarian size as a result of hind-leg removal was substantially greater than the increase in testes size as a result of hind-leg removal.

What does this all mean? The results of this study suggest that life history trade-offs (IN BUGS) may not be based on functional grouping as often assumed. Rather, the trade-off between weapons and testes appear to reflect factors other than functional groupings (i.e., reproduction). Although the results of the male cactus bugs are consistent with the notion that reproductive functions compete for the same pool of resources, the finding of female cactus bugs in this study throw a wrench in the ‘life-history trade-offs are functionally based’ because the females are making trade-offs that transcend functional groupings: survival and reproduction.

Why should this matter, especially to behavioral scientists like myself? Of course this study was done in bugs, and generalizations are heavily cautioned. But, applications of life history theory to humans — which originated in animal studies — is a highly active research area, first gaining traction in the 1980s. The foundations of human life history theory rest on the assumption that the Miller et al. paper challenges: that life history trade-offs are functionally based. The fundamental trade-offs cited in human applications are: (1) current vs. future reproduction, (2) quantity vs. quality of offspring, and (3) matting effort vs. parenting effort. Unfortunately, human studies often rely on survey research rather than experiments such as what can be done with animals. We can’t chop of kids arms, or alter their muscle mass to see whether their gonads are altered as a result. Experimental methods to test key theoretical assumptions are extraordinarily challenging to implement in humans.

Applications of life history theory within the psychological and behavioral sciences have also been under heavy scrutiny, especially in the past few years, being challenged on numerous grounds. One of these criticisms, put forth by Daniel Nettle and Willem Frankenhuis in a paper also published in Proceedings B earlier this year, is that human life history research has become disconnected from its biological and animal foundations since 2010. Their analysis shows that human studies post-2010 are less likely to cite foundational work from animal behavior than earlier work, indicative of the human literature becoming more distanced from its theoretical roots.

Paper published 8 March 2019 in Proceedings B on the life history literature.

It’s has come to light that the human life history literature is a bit of a mess as of late (in my opinion, anyhow). Many old hypotheses are being challenged and theoretical foundations are being questioned.

Given then challenges of experimental life history work in humans & the difficulty of testing theoretical premises underpinning human work, more attention needs to be paid to comparative work that has the methodological ability to do what cannot be done with humans.

Work by Miller et al. is a nice example of why we (behavioral scientists) should be focused on the animal world — to reconnect human life history work with its biological foundations.



Nicole Barbaro, Ph.D.

I hold a Ph.D. in psychology and work in various professional roles in Higher Education. I now write on Substack. Learn more at