Book review – Mate Choice: The Evolution of Sexual Decision Making from Microbes to Humans

I have to preface this review by pointing out that I did not read this book from a fully neutral position. Gil Rosenthal, a professor in biology, ecology and evolutionary biology at Texas A&M University, does mate choice research on fish. So did I. Though he works on live-bearing swordtails and I worked on threespine sticklebacks, some of the work he discusses has been written by people I knew personally as supervisor, co-workers or colleagues. Many more publications referenced are ones I also read during the course of my PhD research. You could say that mate choice research is a field I am, errr, intimately familiar with. At least where fish are concerned. At the same time, I left academia after graduating in 2010, so this book seemed like a good opportunity to get back in touch with this research field.

Anyway. Sex.

“Mate Choice: The Evolution of Sexual Decision Making from Microbes to Humans”, written by Gil G. Rosenthal, published by Princeton University Press, in August 2017 (hardback, 632 pages)

From the beautiful song and dance of birds-of-paradise, the use of spermatophores (i.e. packages of sperm) as nuptial gifts in insects, the sexual cannibalism (i.e. let’s-have-sex-and-then-I’ll-kill-you) in other insects, pregnant seahorse males, the aggregations of displaying males on so-called leks in grouse or certain antelopes, or the broadcast spawning events of certain fish (i.e. free-for-all mating aggregations that turn the waters into a soup of sperm and eggs)… the world of animal courtship and reproduction is endlessly varied and endlessly fascinating. It has given many a pop-science author an excuse to write amusing and slightly racy books, Howard’s Sex on Earth: A Journey Through Nature’s Most Intimate Moments or Schilthuizen’s Nature’s Nether Regions: What the Sex Lives of Bugs, Birds and Beasts Tell Us About Evolution, Biodiversity and Ourselves being just two recent examples. We serious biologists of course read Shuster & Wade’s Mating Systems and Strategies for an overview.

As Rosenthal observes, the downside of all this diversity is a certain “Balkanization”. There are complete research programmes on mate choice in fish, similarly for birds, frogs and humans. But there isn’t necessarily a lot of cross-talk between the various disciplines of e.g. ethology, neurobiology or evolutionary psychology. And the vastness of the associated literature is such that it’s hard to be an expert in all these fields. Rosenthal’s book is a brave attempt to offer a cross-disciplinary, cross-taxonomical overview of mate choice to bring these fields closer together. Even though it’s not intended as an exhaustive literature review, Rosenthal has read thousands of publications, and the reference section of this chunky book runs to some 112 pages (having been printed on heavy paper stock, this is a doorstopper).

The main point Rosenthal wants to make with Mate Choice is that the role of “good genes” is overrated. One school of thought in mate choice research that has received much attention is the idea that during courtship, one sex (often females) picks a partner (often males) based on traits that indicate good genetic quality. She may not directly benefit from this herself, but her offspring will indirectly gain an evolutionary advantage. Though this mechanism has its role, Rosenthal argues it is minor. Decades of research have failed to turn up much direct evidence. As an aside, Rosenthal talks about courters and choosers, rather than males and females. This is not just political correctness; other than sex-role-reversed species, there is increasing evidence for strong female choice on males in some species, and roles switching back and forth between males and females within one interaction.

“[…] the world of animal courtship and reproduction is endlessly varied and endlessly fascinating”

The first part of this book walks through the actual biological process of mate choice. First there is sensory biology. Before you can choose, you need to detect the courtship signal, whether through smell, sound, or sight. Then there is cognition. In reality, most courters pay attention to several signals, and to several features of each signal (e.g. bowerbird females evaluate the male’s bower, his song, his dance, and his plumage). This requires processing and integrating complex information. A courter ends up preferring not just one trait, but a combination of several traits, a so-called multivariate preference. Then there is evaluation, once observed and processed, a courter needs to decide: is she attracted, indifferent, or repelled by this display? Then comes choice. It’s not uncommon for several courters to be vying for a chooser’s attention. Who do you choose? If not, how many partners do you sample before coming to a decision? And it doesn’t stop there, even during and after mating, choice continues. Sperm can be stored or ejected by females, and strategic decisions can be made on how much time and resources to allocate to offspring (collectively this is known as cryptic choice, as it is harder to observe). And of course, courtship is rarely a one-way street, but a dynamic process that involves give and take by both parties, i.e. mutual mate choice. This part of the book is already fascinating, giving many examples of how different and complex mate choice can be in various creatures.

The middle section of the book discusses variation in preferences and choices among species, between individuals and within individuals. Genetic, environmental (e.g. seasonal), and social (e.g. preferences learned from parents) factors play a large and decisive role in determining the outcome of mate choice.

The final section deals with the origin, evolution, and consequences of mate choice. Where do preferences come from? How does natural selection act on them, i.e. how do they evolve? And, the core focus of current research, how do chooser preferences and courter traits evolve together? Finally, Rosenthal considers the role of mate choice in the formation of new species or their disappearance through hybridization.

“[…] choosers do not always mate with the most attractive courter, but rather pick the least worst”

The range of disciplines covered here reveals many striking findings and is an education in mate choice research. Some things that struck me were that choosers do not always mate with the most attractive courter, but rather pick the least worst. Or the idea that mate choice is rarely fully optimized from the chooser’s point of view. Often, the value of a certain preferred trait, or the combination of preferred traits, simply isn’t present in the current population of courters she finds herself in, or even lies outside of the scope of what is biologically possible. This is how biologists came upon the preference for so-called supernormal stimuli, think of Niko Tinbergen’s findings that seagull chicks preferred dummies of seagull beaks that showed exaggerated colour patterns compared to what parent seagulls normally show.

The information-density is high and it reminded me of reading papers when studying. Sometimes I had to read paragraphs several times to get them. I do not say this to criticize Rosenthal’s writing style; I see it as an inescapable consequence of communicating complex, sometimes abstract ideas at a high level. As such, the audience for this book is clearly an academic one. But if you research mate choice, or are starting out, this book is a benchmark work you need to read. Books with such a wide scope aiming to synthesize a field don’t come along very often. That alone makes this book an important contribution, and I, for one, am glad to have read it. I expect this will become a standard reference work, on par with Birkhead & Møller’s Sperm Competition and Sexual Selection, Andersson’s Sexual Selection, and Shuster & Wade’s Mating Systems and Strategies. The last two were also published by Princeton University Press, so I am pleased to see them continuing a tradition of publishing important works in this field.

Disclosure: The publisher provided a review copy of this book. The opinion expressed here is my own, however.

Mate Choice hardback or ebook