Attraction and Selection 3: Display & Epilogue

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Charles Darwin got there first.

Yes, Alfred Russell Wallace was hot on his heels. Yes, Erasmus Darwin had offered a comparable hypothesis (albeit lacking mechanism). Yes, Lynn Margulis championed theories that added lightyears of insight to the story of life…but Charles Darwin got there first.

All us evolutionary wannabes are scrambling to catch up. Every word I’ve written and logical chain I’ve argued in this trilo-blog follows a well-trodden groove that began with The Origin of Species and The Descent of Man, a groove worn smooth by the likes of Julian Huxley, Ronald Fisher, Ernst Mayr, E.O. Wilson, and many others. All that neurotic chatter about muscle mass, male contests, and fancy adornment? It inevitably leads here.

With that in mind, I’ll let Chucky D open this final chapter for me:

The Descent of Man, Chapter 8. Emphasis and pigeons added by me.

The Descent of Man, Chapter 8 [1]. Emphasis and pigeons added by me.

That’s right. Once you’re ornamented and rocking your bling, you need a way to show it off. This last installment on attraction and selection will focus on those marvelous “antics”, or commonly referred to as courtship displays.

Much like adornments, some displays can be practical. If you have ever owned a male Betta fish (Betta splendens), you probably observed it blowing masses of bubbles. Those frothy structures are nests for eggs, and are an important criteria for females searching for a mate [2].

If the sheer number of nests wrens build doesn't unnerve you, the interiors of the nests will. They could make a series called Stick Horders about it.

Marsh Wren, doing the splits. As them Marsh Wrens do.

Nest building is a common courtship component in fish and bird species, and it can get a little out of hand. I once foolishly attempted to monitor a pair of House Wrens (Troglodytes aedon) breeding in my yard, only to discover that the male was building bags of nests, and the female only laid in the ones I didn’t find. This is a trope in the wren family (Troglodytidae). Male Marsh Wrens (Cistothorus palustris) will build as many as 12 nests, only a few of which will receive any use by females. There has been some debate as to whether this overzealous home-building is an advertisement of male quality [3], a function of polygyny [4], or just a way to screw with predators/ornithologists [5]. Whatever the explanation, the building of at least one nest is a signal of a male’s capacity as a parent.

Another example of practical courtship is nuptial feeding. In many insect [6], arachnid [7], and bird species [8], males will woo females with a romantic meals. Male shrikes (Laniidae, one of the gnarliest passerine families out there) maintain “larders” of impaled mice and lizards. Female shrikes prefer males with the most macabre displays, and lay more eggs when males bring the bloody mess right to them [9].

Two perspectives on nuptial feeding.

Two perspectives on nuptial feeding.

Likewise, males of some insect species deliver salts and other sustenance to aid females in egg production. These nuptial gifts can be captured prey, but often take the form of a spermatophore–a nutritional matrix filled with ejaculate that females eat after absorbing the sperm [10]. It’s like a gift with edible wrapping paper, only much grosser.

In arachnids, the role of nuptial feedings is more complicated. While a prey offering may help enrich the eggs the female lays, it’s also conceivable that the male is hoping to just sate the female enough to live and mate another day [11].

The parallels between nest building/nuptial feeding and human behavior are easy to draw. A whole slew of studies have addressed the relationship between male wealth and reproductive success. The selection gradient diminishes somewhat with industrialization [12], but on the whole the wealthiest blokes take the lion’s share of mating opportunities [13, 14, 15]. Alas, my paltry checking account and moldering 403(b) are unlikely to win me any suitors.

Fortunately, many displays don’t require material goods to be found attractive. You could trawl the internet for weeks without running out of videos of exaggerated animal courtship performances (for real). Some displays are simple, like the push-up performance by Sceloporus lizards that show off male’s upper body strength and flashy sides:

So strong. So manly.

Other displays are more complicated, like the tremendous dancing of peacock spiders (Maratus sp.), who have risen to internet fame thanks to Jurgen Otto high-resolution videography.

Other displays seem to be just plain annoying. Male red-eared sliders (Trachemys scripta) will use their long finger claws to repeatedly tap and brush females’ faces. It’s as weird as it sounds. If someone did that to me for 20 minutes, I’d probably mate with them just to get them to lay off.

Shtaaaaaaaaaahp

With such a preponderance of courtship displays, we have to ask: are they a signal of male quality, or merely an invitation to mate? After all, complex displays can function to prevent inter-species mating, allowing both sexes to avoid issues of gametic incompatibility [16, 17]. To ensure that courtship is a sexually selected signal of quality and not just a pre-zygotic barrier to hybridization, we need to determine whether variation in display within species reflects male quality, and in turn translates into female preference.

For our starting example, let’s look at a species familiar to us North Americans: the Song Sparrow (Melospiza melodia). This streaky little creature breeds cross the northern US and Southern Canada, and down California into Baja (range map here).

If you spend time this spring in open fields, you’ll notice that individual sparrows have uniquely variable songs; some males sing several complex songs, while others seem stuck with a few dull melodies.

Zounds! A variable display! So does variation reflect female preference?

song Indeed, captive female Song Sparrows solicit copulations more frequently when exposed to more diverse repertoires of recorded songs in lab settings [18]. Additionally, more diverse song repertoires are predictive of higher reproductive success in wild male Song Sparrows [19], suggesting that repertoire diversity is an honest signal of male quality.

The relationship between male song quality and female preference is well established in many songbird species [2021, 22] and some insects [23, 24]. But what makes song an honest signal of male quality? Much like fluctuating asymmetry, song may reflect a bird’s past. A low-quality bird that couldn’t obtain the calories to grow the neural circuitry, and thus have a smaller song repertoire [25].

The costs of courtship don’t stop at learning displays. Often, the display itself is injurious to the performing. Take wolf spiders: males court females by sending vibrations through the substrate and waving about their heavily tufted forelegs. Female wolf spiders show preference for larger tufts and better vibrations, as demonstrated by simulated males in the Uetz lab in the video below. When researchers induced increased drumming frequency by presenting males with a line-up of females, males rapidly lost weight…and sometimes just plain died of exhaustion [26].

Other examples of display-hard/die-young can be here and here, but perhaps my absolute favorite cost-of-display example is with the Cock-of-the-Rock (Rupicola sp).

An Andean Cock-of-the-Rock (Rupicola peruvianus). Photo by Joel Lisenby, shared under CC BY-SA 3.0

An Andean Cock-of-the-Rock (Rupicola peruvianus). Photo by Joel Lisenby, shared under CC BY-SA 3.0 via Wikimedia

There are two species (give or take) of these South American cotingas: Guianan and Andean. The males are bizarre creatures, searing red or orange with crests that cover their beaks and alien-bright irises; the females are a subdued rust-brown. The species is highly dimorphic in its behavior as well; females raise offspring entirely on their own, and only interact with males when mate-searching. When females are searching, males certainly put on a show.

Cock-of-the-Rocks (or Cocks-of-the-Rock? Cocks-of-the-Rocks?…let’s call ’em COTRs) engage in lek mating: males gather in geographically fixed locations to compete and display for soliciting females. Freed from the demands of parenting, males spend their days preening, strutting, and make a ruckus whenever a single lady shows up.* I really mean ruckus–this is what a lek sounds like when a female kicks it into high gear:

Now, imagine you are a predator wandering the rainforest understory. It’s dark and quiet; most prey items are small and quick, cautiously flitting through shadows. Suddenly, you come upon a lek of screaming, blaze-bright birds entirely focused on showing off.

Turns out this a real consequence for COTR leks. A paper by Pepper W. Trail in 1987 [27] described how frequently male leks would flip out over incoming predators…or flip out because of false alarms. 90% of the times the males fled crashing into the vegetation, it was for false alarms.

Lekkk

Variation in lek size in the Andean Cock-of-the-Rock.*

As if waiting around to holler for a quickie while predators snatch at you from the shadows, mating success in lek species is incredibly skewed: usually one or a few males win most of the paternity in a given breeding season. Seriously, can you image participating in this silly dance for months on end and never getting laid?

Blue Manakin (Chiroxiphia caudata) Lek. Only one guy is gonna be invited to partake in some nookie.

Birds aren’t the only group whose antics draw in the hungry nasties [28, 29]. Male túngara frogs (Physalaemus pustulosus) risk getting snatched by fringed-lipped bats (Trachops cirrhosis) each time they join the chorus [sick imagery of that here and here]. To make matters worse, the complicated calls that females túngara frogs prefer are also preferred by bats.; the better a male sings for ladies, the easier it is for bats to find him [30].

Darwin and most of his successors have seen parallels between the song and dance of the animal kingdom and those of our own species. There are legitimate arguments that our artistic traditions are as much about social bonding as they are about mate selection, and I suspect there’s a lot of truth to that hypothesis [31]. However, the sexually dimorphic registers of human voices [32], females’ increased preference for lower pitches when fertile [33], and the seemingly supernatural allure of guitarists suggest that musical and dancing facility may be yet another signal used in human mate selection.

Also, remember that discussion of fluctuating asymmetry in Part 1? It turns out that there’s a strong relationship between a man’s symmetry and his dancing abilities: more symmetrical dudes have better moves than us Lopsided Larry’s [34]. Moreover, dancing highlights existing asymmetries, such that the attractive power of a man’s shimmy diminishes with increasing physical asymmetry.

If you’ve stuck with me to this point, you know what’s coming next: this is the part where I point out how the cited research indicates my paucity of attractive quality.

Truth be told, I’m not horrible with music; I can carry a tune if need be. But I am an abysmal dancer…think along the lines of Allie Brosh‘s experiences recreating Beyoncé. I spend most of my time in clubs awkwardly shuffling by my lonesome while my boyfriend and friends cut every rug in the joint.

So what’s the point of all this? I’ve burned some 6,000 words highlighting all the ways I cannot be considered attractive from a biological or sexual selection-perspective. Can I say anything to redeem this self-pity party? Isn’t there supposed to be some moral that me and all the fugly uggos can use to lift our spirits?

Of course there is. Next time you’re sitting around, anxious about whether you’re hot enough to make par, or glowering at everyone fitter than you at the gym, take a moment to imagine yourself as you’d like to be. Really indulge yourself. Picture your body, its every angle and curve ideal. Visualize your shape as buxom or lanky, gracile or virile, your every blemish erased–whatever your fantasy is, hold it fully in your mind and really see it.

idealz

Now, without forgetting what that person looked like, summon an image of the people you admire most. Picture all those people–living or dead–you think really matter, people whose approval you strive to obtain, people who you could point to and declare: “This person, they are worthy of emulation!”

right

If you’re even a half-developed human, you didn’t choose your heroes on the basis of sex appeal. Some might as homely as the rest of us mere mortals.

If your idols are handsome, I bet that quality pales in comparison to their other distinctions: brilliance, devotion, compassion, diligence, equanimity, patience, and a hundred other noble elements that contribute to greatness.

Don’t sully these concepts by claiming morality is hot, or that altruism is lush. I know you want to, but don’t. Kindness, perseverance, courage, forgiveness, honesty don’t need to be sexy. They are traits with intrinsic merit.

I guess the moral of the story is this…whether you think of attraction is selected for, or culturally determined, or in the eye of the beholder, the hard truth remains the same: we may never be as attractive as we want to be–no matter what a Dove Commercial says.

All we can do is try our best to not give a fuck because there are much higher aspirations than physical perfection. The unrelenting pursuit of justice, determination to unveil the mysteries of the universe, commitment to serving the least of our brothers–such attributes are the making of true champions.

Dr. Jonas E. Salk, creator of the polio vaccine. Rather than get rich with this creation, Dr. Salk did not patent the vaccine. The lowered cost of production ensured has saved millions of lives. Public Domain Image

Dr. Jonas E. Salk, creator of the polio vaccine. Rather than get rich with this creation, Dr. Salk did not patent the vaccine. The lowered cost of production ensured has saved millions of lives. Public Domain Image.

Among my resolutions for this year is demote being attractive to the lowest of my ambitions. If I could reach into my past to exchange every second of body anxiety for a moment that I took to be kind, or to enrich my mind, or to be creative…heavens, my life would look different today.

So here’s to making life look different. Here’s to tossing aside body dysmorphia and leaving the mad game of sexual selection to creatures who can’t aspire to higher ideals, creatures who have no need of justice or virtue or science.

Besides, they look better displaying than any of us.

Footnote

*If you ever have a chance to visit any kind of lek, I highly recommend it; they are among the most hilarious and transfixing phenomenon in nature. If you’re a North American, you can probably check out a Prairie Chicken lek. However, please be careful and respectful to the lek when you do visit–flushing the displaying males could be energetically costly and lower the quality of the lek site.

**This illustration is a little misleading. The advantage of having a noisier, more vigilant lek are discussed in Pepper paper. But I really wanted to draw a derpy COTR being attacked by a snake, so I did.

Citations

1. C Darwin. 1871. The descent of man, and selection in relation to sex.

2. ED Clotfelter, LJ Curren, and CE Murphy. 2006. Mate choice and spawning size, display behavior, and nest size. Ethology 112(12): 1170-1178.

3. KJ Metz. 1991. The enigma of multiple nest building by male marsh wrens. The Auk 108: 170-173.

4. J Verner and GH Engelsen. 1970. Territories, mutliple nest building, and polygyny in the long-billed marsh wren. The Auk 87(3): 557-567.

5. ML Leonard and J Picman. 1987. The adaptive significance of multiple nest building by male marsh wrens. Animal Behaviour 35(1): 271-277.

6. K Vahed. 1998. The function of nuptial feeding in insects: a review of empirical studies. Biological Review 73(1): 43-78.

7. K Vahed. 2007. All that glistens is not gold: sensory bias, sexual conflict and nuptial feeding in insects and spiders. Ethology 113(2): 105-127.

8. D Lack. 1940. Courtship feeding in birds. The Auk 57(2): 169-178.

9. A Carlson. 1989. Courtship feeding and clutch size in Red-backed Shrikes (Lanius collurio). The American Naturalist 133(3): 454-457.

10. DT Gwynne. 1984. Courtship feeding increases female reproductive success in bushcrickets. Nature 307: 361-363.

11. P Stålhandske. 2001. Nuptial gift in the spider Pisaura mirabilis maintained by sexual selection. 12(6): 691-697.

12. D Nettle and TV Pollet. 2008. Natural selection on male wealth in humans. The American Naturalist 172(5): 658-666.

13. B Pwalwski and RIM Dunbar. 1999. Impact of market value on human mate choice decisions. 266: 281-285.

14. RL Hopcroft. 2006. Sex status, and reproductive success in the contemporary United States. Evolution and Human Behavior

15. T Bereczkei, S Voros, A Gal, and L Bernath. 1996. Resources, attractiveness, family commitment; reproductive decisions in human mate choice. Ethology 103(8): 681-699.

16. WC Davis and VC Twitty. 1964. Courtship behavior and reproductive isolation in the species of Taricha (Amphibia, Caudata). Copeia 4: 601-610.

17. JD Hollander, H Dijkstra, H alleman, L Vlijm. 1973. Courtship behavior as species barrier in Pardosa pullata group (Araneae, Lycosidae). Journal of Arachnology 7: 121-128.

18. WA Searcy, PD McArthur, and K Yasukawa. 1985. Song repertoire size and male quality in Song Sparrows. The Condor 87: 222-228.

19. JM Reid, P Arcese, ALEV Cassidy, SM Hiebert, JNM Smith, PK Stoddard, AB Marr, and LF Keller. 2011. Song repertoire size predicts initial mating success in male song sparrows, Melospiza melodia. Animal Behaviour 68(5): 1055-1063.

20. TI Drăgănoiu, L Nagle, and M Kreutzer. 2002. Directional female preference for an exaggerated male trait in canary (Serinusanaria) song. ProcB 269: 2525-2531. 

21. TQ Getner and SH Hulse. 2000. Female European Starling preference and choice for variation in conspecific male song. Animal Behavior 59(2): 443-458.

22. K Yasukawa, JL Blank, and CB Patterson. 1980. Song repertoires and sexual selection in the Red-winged Blackbird. Behavioral Ecology and Sociobiology 7(3): 233-238.

23. MG Ritchie, RM Townhill, and A Hoikkala. 1998. Female preference for fly song: playback experiments confirm the targets of sexual selection. Animal Behaviour 56(3): 713-717.

24. LW Simmons. 1987. The calling song of the field cricket, Gryllus bimaculatus (de geer): constraints on transmission and its role in inter male competition and female choice. Animal Behaviour 36(2): 38-394.

25. S Nowicki, W Searcy, and S. Peters. 2002. Brain development, song learning, and mate choice in birds: a review and experimental test of the “nutritional stress hypothesis”. Journal of Comparative Physiology A 188(11-12): 1003-1014.

26. J Mappes, RV Alatalo, J Kotiaho, and S Parri. 1996. Viability costs of condition-dependent sexual male display in a drumming wolf spider. ProcB

27. PW Trail. 1987. Predation and anti predator behavior at Guianan Cock-of-the-Rock leks. The Auk 104(3): 496-507.

28. C Magnhagen. 1991. Predation risk as a cost reproduction. TREE 6(6): 183-186.

29. T Ulmar Grafe. 1997. Costs and benefits of mate choice in the lek-breeding reed frog, Hyperolius marmoratus. Animal Behaviour 53(5): 1103-1117.

30. XE Bernal, AS Rand, and MJ Ryan. 2007. Sexual differences in the behavioral response of túngara frogs, Physalaemus pustulosus, to cues associated with increased predation risk. Ethology 113(8): 755-763.

31. EH Hagen and GA Bryant. 2003. Music and dance as a coalition signaling system. Human Nature 14(1): 21-51.

32. S Evans, N Neave, and D Wakelin. 2006. Relationships between vocal characteristics and body size and shape in human males: An evolution explanation for a deep male voice. Biological Psychology 72(2): 160-163.

33. DA Puts. 2005. Mating context and menstrual phase affect women’s preference for male voice pitch. Evolution and Human Behavior 26(5): 388-397.

34. WM Vrown, L Cronk, K Grochow, A Jacobson, CK Liu, Z Popovic, and R Trivers. 2005. Dance reveals symmetry especially in young men. Nature 438: 1148-1150.

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Attraction and Selection 2: Ornaments & Orientation

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Welcome back to my illustrated reflective trifecta on sexual selection and self-perception!

Last time, I nattered on about about how attraction could be trait with evolutionary underpinnings, and used swallow tails and human faces as examples of fluctuating asymmetry’s role in mate selection. In both cases, it was male quality being assessed by females.

I would be remiss if I didn’t acknowledge that all three of these posts will be male-centric. I know, I know–classic paternalistic, chauvinist, phallus-gazing twaddle. Biology’s progress has long been hampered by men whose hypotheses [1], observations [2], conclusions [3], and laboratory culture [4] are warped by machismo. By only emphasizing studies investigating male aspects of selection studies, I contribute to prevailing perception that evolutionary biology is all about teh menz.

Actually, we sometimes ignore males all together in population ecology. This isn't a feminist conspiracy, it's just modeling practicality. Endosymbiosis, however, is a feminist conspiracy.

Actually, we sometimes ignore males all together in population ecology. This isn’t a feminist conspiracy, it’s just modeling practicality. Endosymbiosis, however, is a feminist conspiracy.

Moreover, culturally-reinforced body dysmorphia (my initial writing prompt) disproportionately affects women [5]. Anorexia and bulimia nervosa, while increasingly common in men [6], remain more prevalent among women [7], both domestically [8] and globally [9]. Male body insecurity may seem a small issue by comparison, like panicking about dolphins in tuna when we should be worried about tuna’s inevitable demise (PUT THE SANDWICH DOWN!). But all problems are relative, and body image issues are particularly salient for a subset of the male population: namely, the queer subset.

This isn’t news within the queer community, or among our straight allies. Or our antagonists, come to think of it. Gay body fascism has been part of the LGBTQ lexicon since at least the 1990s*, and has been written about critically by plenty of wise people. The most humorous and human writing regarding the subject can be found on Orlando Soria’s brilliant Homemaker blog.**

Our obsession with being either whip thin or hugely muscular (or both at the same time) is more than an irritating facet of gay culture. Higher body dissatisfaction in young gay men [10 & 11] leads to engagement in dangerous conditions and habits, including eating disorders [12] and anabolic steroid use [13]. Alarmingly, abuse of un-prescripted steroids*** is increasingly prevalent among gay adolescents [14].

Self-endangering practices and self-loathing may be partially attributable to our narcism. However, particularly in the case of teens, I am concerned that body fixation originates as overcompensation, a desire to “make up” for any lack of masculinity we imagine comes free-of-charge with our same-sex attraction.§

But what exactly constitutes masculinity? What is a masculine trait? Symmetry may be a trait by which mates assess males, but it is not a feature exclusive to males. To examine masculine traits, we first need to talk about sexual dimorphism, starting with the obvious.

Males and females of non-hermaphroditic (specifically, non-concurrently hermaphroditic) animals differ in their anatomy. Females must have the facility to produce ova, males the capacity for sperm production. The structures designed to produce, nurture, and deliver gametes are referred to as primary sexual characteristics, and present just a minimum of sexual dimorphism.

In addition to their reproductive organs, the sexes can differ in size, shape, life-span, coloration, vocalization, temperature preference–you name it. All these characteristics are called secondary sexual characteristics. The greater the additive dissimilarity of these secondary characteristics, the more sexually dimorphic we consider a species to be. Additionally, variation in the degree of physical dimorphism within a given clade can illuminate evolutionary trends in mating strategy.

A cursorial examination of how female/male body size dimorphism correlates to mating strategy in apes and pinnipeds. As size dimorphism increases, it appears that the number of females that share single male as sperm donor increases (polygyny increases as Mf/Mm decreases). I made this with an Encyclopedia of mammals as my guide, so it's really not something you can reference as real, but here are some papers about it.

A cursorial examination of how female/male body size dimorphism correlates to mating strategy in apes and pinnipeds. As size dimorphism increases, it appears that the number of females that share single male as sperm donor increases (i.e., polygyny increases as Mf/Mm decreases). I made this with an Encyclopedia of Mammals as my guide, so it’s really not something you can reference, but here are some papers about it.

Let’s consider secondary sex characteristics that contributes strongly to dimorphism as a standard for masculinity. The more a prominent a trait is in males relative to females, the more more masculine we’ll consider it.

What about the size dimorphism in the illustration above? I was initially skeptical of this idea…mostly because I think short men are hot. However, a few conversations and a walk around the Internet provided disturbing evidence that many people do equate height with masculinity. Check out the Heightism Exposed Twitter feed some time. Exempli gratia:

…or…

Not everyone’s a hater, though. I’m not the only person out there who appreciates short men. Besides, smaller-framed men live longer, healthier lives than their larger counterparts [15], potentially allowing for more mating opportunities. [This is extravagant and erroneous supposition, but just run with it for now.]

Also, size dimorphism may be an example of males and females occupying separate ecological niches. This reduces resource competition between the sexes (intersexual competition) [16]. For example, male birds of prey are frequently smaller than the females [17], which reduces the overlap for preferred prey items and allows the larger female–nearly always the primary incubator–to be scary-as-hades. In a similar vein, the sexually dimorphic bills of recently extinct Huia (Heteralocha acutirostris) [18] and extant Green Woodhoopoe (Phoeniculus purpureus) [19] are hypothesized to allow for the males and females to forage for different invertebrates.

Note that the Green Hoopoe bill partitions based on size, while the Huia partitions/ed by size and shape.

Note that the Green Hoopoe bill partitions based on size, while the Huia partitions/ed by size and shape.

If we set aside niche-partioning traits (that is, any trait that could serve to reduce intersexual, intraspecific competition), what secondary sex characteristics does that leave us with as our benchmarks for masculinity? What if we only look at dimorphic traits that serve no other function than the attraction of and competition for mates?

Enter the the wondrous and incredible world of Male Adornment. Examples of sexual ornamentation abound in the animal kingdom. It would be impossible to cover all their variety here: wild colorationcumbersome plumage,  fleshy crests, seasonal antlers, aggressive eyestalks, and so on.

Sometimes, these ornaments look really gross.

The evolutionary path seems relatively straightforward for some of these traits. For males that physically compete for mates, structures that give an advantage in virile brawls will be selected for over time. The enlarged mandibles of stage beetles (Lucanidae), the more elaborate antlers in Cervidae (deer and their allies), and the massive horns of bighorn sheep (Ovis canadensis) all fall under this category.

The selective path for other ornaments is not so clear. Rather than being practical, sometimes sexual adornments seem damn inconvenient, or downright dangerous. For example, what’s the benefit of adding drag to your wings when you forage for flying insects?

Pennant-winged Nightjar (Caprimulgus vexillarius). Illustration originally published in Ibis 1863. © Wikimedia Commons

Pennant-winged Nightjar (Caprimulgus vexillarius). Illustration by Joseph Wolf originally published in Ibis 1863. © Wikimedia Commons

Why would the male of a tiny prey species adorn itself with bright colors that make them look tastier to predators [20]?

Female (left) and male (right) guppy (Poecilia reticulata). Doesn't that orange tail make him look scrumptious?  © Wikimedia Commons

Female (left) and male (right) guppy (Poecilia reticulata). Doesn’t that orange tail make him look scrumptious? © Wikimedia Commons

And seriously, what’s the point of the Narwhal’s tusk? Yeah, I know people claim they’re for sparring or breaking ice, but they are way too long for that bag. With only some inferential evidence [21], I’m going to categorize the tusk as another weird-ass, inconvenient, and possibly maladaptive secondary sexual characteristic.

Ronald A. Fischer, Public Domain image.

Ronald A. Fischer, Public Domain image.

We refer to these bizarre traits as Fisherian Runaways, and the process that created them as runaway sexual selection. They take their name from Sir Ronald Fisher, a prominent evolutionary biologist and statistician (and eugenicist†) in the early 1900s. Fisher was fascinated with these runaway traits–why didn’t natural selection eliminate ornaments that posed such hazards? Wouldn’t the expense of maintaining the trait select against it? The literature on this is enormous, but here are two of the most studied (& not mutually exclusive) hypotheses advanced to explain Fisherian Runaways.

1: Sexy Sons

Female choice for a trait with selective benefits leads to its outsize exaggeration [22]. To use an example from last time, let’s say, many generations past, the outer retrices of the Barn Swallow (Hirundo rustica) were good predictors of flight performance. Slightly longer tail feathers made males more maneuverable, and females that preferred longer-tailed males had fitter offspring. Thus, female preference for this trait is selected for in subsequent generations. After a while, the preference for long outer retrices is ubiquitous and indiscriminate: females will always mate with the male with the longest tail, even when the feathers are so long they don’t confer any flight benefit, and are actually energetically expensive to maintain. Fisher hypothesized that–at some point–the trait runs up against its absolute maximum (when males just die because of it), and is maintained there, with females choosing the fathers that will give her the sexiest sonsmoreswallows

2: Honest Signal

Runaway traits are a honest signal of fitness BECAUSE they are expensive [23]. Sure, a male guppy’s bright colors require energy to maintain, and make it susceptible to predation. But if a male survives in spite of these costs, a female knows he’s fit enough to forage well and dodge predators. Thus, choosing the male with the most outsize ornamentation leads to fitter offspring over generations, and the ornament is maintained.

Even though fewer showy males survived predation events, the ones that do may have that "extra something" to contribute to offspring fitness.

Even though fewer showy males survived predation events, the ones that do may have that “extra something” to contribute to offspring fitness.

We’ll return to runaway traits again in Part 3, but for now let’s look to humans and whether or now we can be considered ornamented. Some of our dimorphism is reproductive practicality, like women’s broadened hips for child-bearing. Some of it may be due to physical intrasexual conflict–at least, this hypothesis has been advanced to explain men’s thickened face bones (I guess our grandfathers have been bashing each other in the faces for a long time [24]).

What ornaments do we have that serve no real purpose? One could argue that humans’ pendulous mammary glands (boobs) are strictly ornamental prior to lactation, but that’s complicated by our evolutionary history as extended breastfeeders [25]: pre-childbirth breasts could have originated as a signal (honest or otherwise) of the potential to feed infants.

To me, that leaves one glaringly obvious dimorphic trait; one that appears to serve no real purpose than to populate cafes and artisan doughnut shops in every hipster-mecca across the globe, that bizarre and variable aspect of the male pubescence: the beard.

This is the dominant phenotype for Richmond males aged 25-35. Photo by Juan Luis, shared under Creative Commons License.

This is the dominant phenotype for RVA males aged 25-35. Photo by Juan Luis, shared under Creative Commons License.

I’ve searched Web of Science and Google Scholar using the terms “beard”, “evolution”, “facial hair”, “Homo sapiens“, “male”, “mustache”, “selection”, and “female preference” in various combinations. To my surprise, there isn’t much consensus on when facial hair evolved in humans, or what conditions selected for it, perhaps because beards themselves are so variable.††

Most hypotheses regarding their function fall along these lines:

  1. Beards were face insulation during the last glacial maximum.
  2. Beards act as wicks and traps for pheromones.
  3. Beards are an intra-sexual (i.e., man-to-man) signal of age & dominance.
  4. Beards function as inter-sexual (man-to-woman) of mate quality (i.e., good genes/sperm).
  5. Beards are an inter-sexual signal of social quality (i.e, socially dominant, with resources to be a providing father), but not gene quality.
Evolution. Why beards? What beards do? Many hypotheses. Much conjecture.

Dear Evolution: Why beards? What beards do? Many hypotheses. Much conjecture. Love, Dan

Hypothesis 1 is dumb. Women were exposed to the same frigid conditions as men during the Pleistocene, and they didn’t evolve beards.

Hypothesis 2 may be less dumb, but beard hair, which is long and relatively straight, doesn’t share the physical characteristics with pheromone-wicking pubic hair, which is short and curly.

Hypothesis 3 may have something to it. I do feel an abnormal compunction to punch hipsters in the ironic beard when they bring up their NGO that teaches low-income urban youth to brew kombucha using mason jars and cultures from moldy single-speed bicycle seats.

But hypotheses 4 & 5 are where most behavioral research has focused. Findings have been pretty variable. In some cases, women identified beards as unattractive [26], or only signaling age and dominance [27]. In others, women did find stubble unusually attractive, particularly when most fertile [28]. One study even found weak evidence that preference for beards is genetic, with monozygotic (identical) twins’ sharing attraction to facial hair more often that dizygotic (fraternal) twins [29].

The current popular study attributes this variable beard attraction to negative frequency-dependent preferences, or NDFPs. If a trait is subject to negative frequency-dependent preference, its allure is inversely related to its prevalence. In other words, the more common a trait is, the less sexy it becomes.

NDFP has been used to explain how the variety of colorful guppy tails is maintained in wild populations [30, 31, 32]. If we expect preference for only one tail type, the others would disappear from the population in a few generations. However, if females preferentially mate with the least common tail type–or males with tails different from previous mates–the proportion of tail types will fluctuate over time, maintaining the population’s polymorphism. [Predation has a hand in this, too]

Negative frequency-dependent preference in action, in guppies, in love.

Negative frequency-dependent preference in action, in guppies, in love.

Janif et al. (2014) demonstrated that attraction to male beards my operate on a similar principle [33]. To do this, they showed women (and men) photographs of men’s faces with a range of facial hair, and had the participants rate their attraction to those faces. Additionally, researchers manipulated the proportion of beardy faces that participants viewed. Some participants saw lots of stubble, others saw lots of clean-shaven faces, while others primarily saw of bearded countenances.

Participants ended up rating the phenotype they saw less frequently as more attractive. If they were exposed to many clean-shaven faces, they rated the bearded faces as more attractive. If there were plenty of beards, they perceived the hairless chins as sexy.

Janif et al. (2014) study, recreated with unauthorized sketches of my boyfriend. He normally sports designer stubble.

Janif et al. (2014) study, recreated with unauthorized sketches of my boyfriend. He normally sports designer stubble.

So good news for men everywhere! To figure out what facial hair is currently sexiest, you just need to quantify polymorphisms around you. Go with the least abundant variety, and you’ll be the belle of the ball. Or the beaux of the ball.

That is, unless you’re like me. While my father and younger brother both sport healthy beards, I think my Y-chromosome was baked at the wrong temperature. I can go about 5-6 days without shaving, with my face staying relatively smooth. Sometime around day 7, hideous tufts of red-brown wire erupt in uneven patches from my jaw and upper lip. To add insult to injury, it itches something fierce.

bearaaah

Alas, another masculine trait not available to me. But never, fear–phenotype is so much more than anatomical structures. A great wealth of phenotype can be found in behavior. More on that in Part 3.

FOOTNOTES

*The earliest use of the term “body fascism” in reference to gay workout and physical norms I can find is a Guardian article by Richard Smith on 1993.10.23 titled THINGS THAT GO PUMP IN THE NIGHT: More gay man hours are spent in the gym than the nightclub. Why? Because muscle has pulling power. (1) Gosh, I love rambling headlines. (2) Gosh, I love bad puns & Aerosmith references. (3) Gosh, I would love to link to this article as well as the author’s website, but I found it through Lexis Nexus, and several men with the name of Richard Smith write for the Guardian, and I can’t be sure which one penned this paper. If you know who/where he can be found, let me know and I’ll hyperlink to him.

**Mr. Soria sarcastically concludes saying that body obsession will lead gay men to inherit the earth. They will, but not because of any mental or physical superiority. The Queer Illuminati have powers beyond heterosexuals’ wildest imaginings.

***Anabolic steroids have legitimate medical uses, treating hormone deficiencies, weight loss from cancer, and wasting associated with AIDS.Turns out queer guys are much more likely §Not saying feminine or non-masculine guys ain’t great. We are. The issue is that we think we ain’t.

† Yes, once upon a time, many brilliant people were ardent eugenicists. Yes, there was a journal called Eugenics Review, and it occasionally published papers with reputable science. I’m working on a post about the frightening history of eugenics & evolutionary biologists, but for now, I’ll leave it at this: eugenics is a monstrous and evil philosophy. It mixed scientific theory with myopic, classist, and racist perceptions of society to create reprehensible policy.

††Facial hair is a variable trait between populations: Mediterranean populations are notoriously hirsute, while facial hair is considerably dense and abundant in some East Asian lineages. We can’t be certain of the evolutionary history for each of these populations, and thus our inferential power is limited.

CITATIONS

1. PA Gotway. 1992. Evolutionary biology and feminism. Human Nature 3(3): 217-249.

2. PA Gotway. 2003. Sexual natures: how feminism changed evolutionary biology. Signs 28(3): 901-921.

3. WB Eberhard. 1990. Inadvertent machismo? TREE 5(8): 263.

4. BB Spanier. 1995. Im/partial science: gender ideology in molecular biology. Indiana University Press, Bloomington, IN, USA.

5. JL Muth and TF Cash. 1997. Body-image attitudes: what difference does gender make? Journal of Applied Psychology 27(16): 1438-1452.

6. A Raevuori, A Keski-Rahkonen, and HW Hoek. 2014. A review of eating disorders in males. 27(6): 426-430.

7. LKG Hsu. 1989. The gender gap in eating disorders: why are the eating disorders more common among women? Clinical Psychology Review 9(3): 393-407.

8. RH Striegel-Moore, FA Dohm, HC Kraemer, CB Taylor, S Daniels, PB Crawford, and GB Schreiber. 2003.  Eating disorders in white and black women. American Journal of Psychiatry 160(7): 1326-1331.

9. KM Pike, HW Hoek, and PE Dunne. 2014. Cultural trends in eating disorders. Current Opinion in Psychiatry 27(6): 436-442.

10. GS Jankowski, PC Diedrichs, and E Halliwell. 2014. Can appearance conversations explain differences between gay and heterosexual men’s body dissatisfaction? Psycology of Men and Masculinity 15(1): 68-77.

11. J Brown, D Graham. 2008. Body satisfaction in gym-active males: an exploration of sexuality, gender, and narcissism. Sex Roles 59(1-2): 94-106.

12. CJ Russell and PK Keel. 2002. Homosexuality as a specific risk factor for eating disorders in men. International Journal of Eating Disorders 31(3): 300-306.

13. DR McCreary. 2007. A review of body image influences on Men’s fitness goals and supplement use. American Journal of Men’s Health 1(4): 307-316.

14. AJ Blashill and SS Safren. 2014. Sexual orientation and anabolic-androgenic steroids in US adolescent boys. Pediatrics 133(3): 469-475.

15. TT Samaras and H Elrick. 2002. Height, body size, and longevity: is smaller better for the human body?  West J Med 176(3): 206-208.

16. RK Selander. 1966. Sexual dimorphism and differential niche utilization in birds. The Condor 68(2): 113-151.

17. M Andersson and RÅ Norberg. 1981. Evolultion of reversed sexualBiological Journal of the Linnean Society 15(2): 105-130.

18. DM Lambert, LD Shepherd, L Huynen, G Beans-Picón, GH Walter, and CD Millar. PLoS ONE 4(11): e8019.

19. AN Radford and MA du Plessis. Bill dimorphism and niche partitioning in the Green Woodhoopoe. Journal of Animal Ecology 72(2): 258-269.

20. J-GJ Godin and HE McDonough. 2003. Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait. Behavioral Ecology 14(2): 194-200.

21. TC Kelley, REA Stewart, DJ Yurkowski, A Ryan, and SH Ferguson. 2014. Mating ecology of beluga (Delphinapterus leucas) and narwhal (Monodon monoceros) as estimated by reproductive tract metrics. Marine Mammal Science (Early View).

22. RA Fisher. 1915. The evolution of sexual preference. Eugenics Review 7(3): 184-192. †

23. H Kokko, R Brooks, JM McNamara and AI Houston. 2002. The sexual selection continuum. ProcB 282: 1331-1340.

24. DR Carrier and MH Morgan. 2014. Protective buttressing of the hominin face. Biological Reviews: Early view.

25. LT Humphrey. 2010. Weaning behavior in human evolution. Seminars in Cell & Developmental Biology 21(4): 453-461.

26. B Dixson, P Vasey, and R Brooks. 2013. The evolution of the human beard. Journal of Comparative Human Biology 64(2): 146.

27. F Muscarella and MR Cunningham. 2013. The evolutionary significance and social perception of male pattern baldness and facial hair. 17(2): 99-117.

28. BJ Dixson, JC Tam, M Awasthy. 2012. Do women’s preferences for men’s facial hair change with reproductive status? Behavioral Ecology ?

29. VJH Verwein, AV Burri, BP Zietsch. 2012. Evidence for genetic variation in human mate preferences for sexually dimorphic physical traits. PLOS One 7(11): e49294.

30. M Andersson. 1986. Evolution of condition-dependent sex ornaments and mating preferences: sexual selection based on viability differences. Evolution 40(4): 804-816.

31. R Brooks. 2002. Variation in female mate choice within guppy populations: population maintenance. Genetica 116(2-3): 343-358.

32. AL Eakley and AE Houde. 2004. Possible role of female discrimination against ‘redundant’ males in the evolution of color pattern polymorphism in guppies. ProcB 282(1801): S299-S301.

33. ZJ Janif, RC Brooks, and BJ Dixson. 2015. Negative frequency-dependent preferences and variation in male facial hair. Biology Letters 11(1): 1-4.

Attraction and Selection 1: Prologue & Symmetry

Standard

This biological soliloquy (in 3 parts) is brought to you by Pine Street Barbershop. More accurately, it started with my visiting said barbershop to request a trendy haircut.

1

I’ve worn my hair in an unruly mop for the last ten years, chopping back the thin curls when they entangle my ears. With male pattern baldness setting in, I decided a few weeks ago that I may as well try to look hip while my follicles still work.

Thus resolved, I marched into Oregon Hill and asked for an undercut. Lots of handsome people seem to have them, and anything that makes me more like Robyn is a good style choice in my book.

The buzzers sheared away the hair from back and sides of my skull, every lock I lost bringing me closer to cool. After paying the barber, I strolled over to the gym for my daily workout, pleased with how refreshing the breeze felt on my exposed temples. It wasn’t until I got to the weight-room floor that I realized something was horribly amiss. Whimpering through a set of dumbbell curls, I glanced in the mirror and beheld the sad truth:

3

There were 800 people at the gym with this haircut, but I can only be bothered to draw two in addition to myself. For real.

I had the same haircut as everyone else at the gym. More importantly, it looked way better on them.

Mostly because they were hot.

Being the scrawniest kid at the gym is not a new experience for me. I remind myself that people come in all shapes and sizes, and that there many ways to be beautiful. Like every other liberal, my Facebook feed is littered with friends posting progressive, body-positive articles, and I read a fair number of them. When I attempt to internalize the blogosphere’s collective encouragements to myself, a conversation like the this ensues:

Dan: It’s okay that I have creepy skinny bird limbs. That can be attractive. I’m still attractive.

Inner Biologist: Do you have any evidence to suggest that?

Dan: If I had the resources, I could recruit 100 volunteers and measure self-reported arousal–

Inner Biologist: Shut up, that’s stupid and gross. The data already exist. People like muscles.

Dan: What?

Inner Biologist: A man’s lean muscle mass is a strong predictor of his number of lifetime sexual partners [1]. People bonk people they find attractive. A trait associated with a better bonk-score is more attractive. This suggests your lack of muscle shouldn’t be considered attractive.

Therein rests the heart of the matter: I can’t bring myself to believe “attraction” as 100% culturally defined, or solely an expression of personal preference (although it is in part both of these things). I’m convinced–perhaps erroneously–that attraction is an expressed trait with at least some biological underpinnings. This trait has been shaped by generations of sexual selection [2], in which fit individuals correctly identified other fit individuals, swapped some genes (and body fluid), and produced fit babies. The babies that inherited their parents’ keen eye for quality genetic merchandise eventually hit adolescence, started feeling/expressing attraction, and made their own fit babies.

What about offspring who didn’t inherit such preferences and chose less-than-fit mates? They produced tragic babies with weird genes. Those babies got selected against, with Grim Selector (i.e., Charles Darwin with a scythe) showing up and removing them from the gene pool.

That attraction to lean muscle mass in men? It’s been selected for, and it’s here to stay.

The Grim Selector. Only distinguishable by the Grim Proletariat by hairline and reading material.

The Grim Selector. Only distinguishable from the Grim Proletariat by hairline and reading material.

Now, you could argue that lean muscle mass is only one trait, inferring some–but not all–adaptive benefits. You might want a mate that is intelligent or has a good immune system in addition to upper body strength. An organism’s fitness results from thousands of traits interacting with a given environment. Wouldn’t it be useful if there were one trait trait that signaled general fitness?

Turns out, there might just be such a trait for us bilaterally symmetrical organisms [3]! Organisms are rarely 100% symmetrical externally (even less so internally, but ignore that right now). Small, random perturbations from left-right symmetry are referred to as fluctuating asymmetry [4]. Prevailing theory holds that these deviations from bilateral symmetry result from the events and challenges an organisms faces during development.

Missed a few meals in the middle of a growth spurt? That shortage of nutrients could mean only your left arm bulks up. Lived in a crappy environment when your teeth were coming in? Better invest in a retainer or risk a snaggletooth smile (at least if you’re a shrew [5]). From parasite infections [6] to intolerable temperatures [7], an adult’s traumatic past can be writ small in asymmetries accumulated over their youth.

Of course, not every asymmetry indicates lower fitness. Additional examples of adaptive asymmetry here and here.

Of course, not every asymmetry indicates lower fitness. Some other examples of adaptive asymmetry here and here.

Some of these stresses may be random; an organism was just in the wrong place at the wrong time. However, other asymmetry-inducing stresses could mitigated by higher-quality traits. For example, more efficient foraging could lead to better feeding even in times of scarcity. Better dispersal abilities could move the organism away from a crappy environment. A stronger immune system could keep parasite levels low. And so on. Thus, fluctuating asymmetry might be an honest signal of mate quality, and organisms that recognize and select more symmetrical mates may pass on better genes to their offspring [8].

There is substantial empirical evidence for this hypothesis (and some against [9, 10]), but the seminal paper that everyone and their mom cite was published in 1992 on Barn Swallows (Hirundo rustica). A scientist by the name of Anders Pape Møller* conducted a study [11] in which he manipulated the symmetry of males’ long outer tail feathers (known as retrices in ornithological circles). Møller clipped the ends tips off, then re-attached them in a fashion that induced asymmetry through shortening/elongation, or maintained symmetry for controls. Møller then observed the reproductive behavior and success of these males throughout the breeding season.

The genus name for Barn Swallow comes from the Latin word for swallow "Hirundo", which also means "flying fish". The Romans weren't particularly with wildlife identification.

The genus name for Barn Swallow comes from the Latin word for swallow “Hirundo”, which also means “flying fish”. Romans weren’t particularly gifted at wildlife science.

The results? The asymmetrical males (particularly those made asymmetrical through shortening) took longer to attract a mate, had later & smaller clutches, and fledged fewer offspring compared to the more symmetrical controls. Females appeared to evaluate males by how symmetrical they were, even though their wonky tails didn’t affect flight performance. Moreover, females invested less reproductive effort if they ended up with a lopsided fellow.

2

A tough reality to swallow.

There are any number of morphological features that can be used to evaluate symmetry. I’ve observed variation in the charismatic face patterns in the population of Golden-winged Warblers I study. Some male’s bibs seem uneven, and others have white “beauty marks” below one eye but not the other. I’ve often wondered if females make mate decisions based on the symmetry of such features.

Screen Shot 2015-01-06 at 2.17.21 PM

Slightly asymmetric male Golden-winged Warbler from Highland County. Don’t get me wrong, I think this guy is gorgeous…but I’m not the one he’s needs to woo.

Speaking of faces and symmetry, let’s talk about Homo sapiens. Humans are face-centric organisms: we have an incredible memory for faces, and focus more on faces than any other feature. It’s not surprising that the symmetry of one’s face can influence how attractive one is perceived [12, 13, 14, 15, and a lot of other studies] or response to their bedroom performance [16].

My favorite paper on this topic was published by Little et al. in 2007 [17], in which scientists measured symmetry preference at different stages of women’s menstrual cycles and among women with different relationship statuses. The researchers found that women showed increased preference for symmetrical faces during peak fertility: the phase in which the genetic quality of the sexual partner mattered most.** Additionally, partnered women showed a much stronger preference for symmetrical faces than un-partnered women. The evolutionary hypothesis generated by this finding? If already partnered, a woman’s investment in an extra-pair fertilization is only worth it if the genes contributed are of high quality, or at least higher quality than her current partner. If un-partnered, it may be better to accept low-quality genes than to miss out on the opportunity to reproduce.***

Being attractive to women who are biologically primed to conceive isn’t my top objective right now. I lack the income to support a family, and I’m quite content with my current boyfriend. In spite of this, I compulsively compare my face against the men I encounter both in person and in the media. The resulting continuum does not inspire confidence.

faces

If my boyfriend were geographically this close to Tom Daley, his expression would possess more predatory hunger.

But hey, symmetry isn’t the only signal of fitness. There are plenty of other traits that may elicit attraction, and my tiny arms and lopsided face may be outweighed by other features.

More on that in Part 2.

*I am aware of the controversy surrounding some of Dr. Møller’s research, particularly the heritability of asymmetry. The 1992 Nature paper described above, to the best of my knowledge, remains debated but un-retracted.

**Humans copulate for lots of reasons, like social bonding [18] or because the TV’s not working [19]. That being said, sexual behavior and attraction appears to change during peak fertility, both for the woman ovulating [20] and the men she interacts with [21].

***This verbiage is always troubling, as it implies that everyone wants a baby on some level, even if it’s not a conscious one. I write this post with the knowledge that human evolutionary behavior and sociobiology are fraught topics with famous critics. We are legitimately concerned with how our perceptions are shaped by culture, and how these perceptions generate bad hypotheses, ugly studies, and erroneous conclusions. So be it.

Citations:

1. WD Lassek and SJC Gaulin. 2009. Costs and benefits of fat-free muscle mass in men: relationship to mating success, dietary requirements, and native immunity. Evolution and Human Behavior 30(5): 322-328.

2. P Brennan. 2010. Sexual Selection. Nature Education Knowledge 3(10):79.

3. Bilateral (left/right) symmetry. Understanding Evolution. <http://evolution.berkeley.edu/evolibrary/article/arthropods_04>

4. L Van Valen. 1962. A study of fluctuating asymmetry. Evolution. 16(2): 125-142.

5. AV Badyaev, KR Foresman, and MV Fernandes. 2000. Stress and developmental stability: vegetation removal causes increased fluctuating asymmetry in shrews. Ecology 81(2): 336-345.

6.  AP Møller. Parasites differentially increase the degree of fluctuating asymmetry in secondary sexual characters. Journal of Evolutionary Biology 5(4): 691-699.

7. TR Gest, MI Siegel, and J Anistranski. 1986. The long bones of neonatal rats stressed by cold, heat, and noise exhibit increased fluctuating asymmetry. Growth 50(3): 385-389.

8. AP Møller and A Pomiankowski. 1993. Fluctuating asymmetry and sexual selection. Genetica 89(1): 267-279.

9. RA Palmer. 1998. Detecting publication bias in meta-analyses: a case study of fluctuating asymmetry and sexual selection. The American Naturalist 154(2): 220-233.

10. T Bjorksten, P David, A Pomiankowski, and K Fowler. 2000. Fluctuating asymmetry of sexual and nonsexual traits in stalk-eyed flies:  a poor indicator of developmental stress and genetic quality. Journal of Evolutionary Biology 13: 89-97.

11. AP Møller. 1992. Female swallow preference for symmetrical male sexual ornaments. Nature 357: 238-240.

12. SW Gangestad, R Thornhill, and RA Yeo. 1993. Facial attractiveness, developmental stability, and fluctuating asymmetry. Ethology and Sociobiology 15(2): 73-85.

13. R Thornhill and SW Gangestad. 1993. Human facial beauty. Human Nature 4(3): 237-269.

14. K Grammer and R Thornhill. 1994. Human (Homo sapiens) facial attractiveness and sexual selection: the role of symmetry and averageness. Journal of Comparative Psychology 108(3): 233-242.

15. N Koehler, LW Simmons, G Rhodes, and M Peters. 2004. The relationship between sexual dimorphism in human faces and fluctuating asymmetry. ProcB 271: S233-S236.

16. R Thornhill, SW Gangestad, and R Comer. 1995. Human female orgasm and mate fluctuating asymmetry. Animal Behavior 50(6): 1601-1615.

17. AC Little, BC Jones, DM Burt, and DI Perret. 2007. Preference for symmetry in faces change across the menstrual cycle. Behavioral Psychology 76(3): 209-216.

18. RJ Levin. 2002. The physiology of sexual arousal in the human female: a recreational and procreational synthesis. Archives of Sexual Behavior 31(5): 405-411.

19. S Whitelocks. 2013. The blackout baby boom! Hurricane Sand to spark 30% rise in births this summer after October power outage left cupels with little else to do. Daily Mail 2013-Feb-28.

20. SW Gangestad and R Thornhill. 2008. Human oestrus. ProcB 275: 991-1000.

21. SC Roberts, J Havlicek, J Flegr, M Hruskova, AC Little, BC Jones, and DI Perrett. 2004. Female facial attractiveness increases during the fertile phase of the menstrual cycle. ProcB 271: S270-S272.