Donna Maney and colleagues report that
the evolution of complex mating strategies are linked to changes in the gene for the estrogen receptor. Changes in one gene can predispose birds toward a “parental investment strategy” (low levels of competition, high levels of parental care) or a “mating strategy” (high levels of competition, low levels of parental care and exta-pair matings).
That in itself is remarkable, but there is another twist. The birds with the genetic change linked to more aggression and less parental behavior almost invariably mate with birds carrying the other genetic arrangement! We knew that both strategies have their advantages, but now it appears that
the two strategies might be complementary when they occur together in the same couple. One member of the pair is more aggressive and territorial, while the other tends to the nest. In pairs where the male takes on more parental duty, the female is likely to be the one who is more aggressive.
Genes and Behavior
Most people agree that our genes affect some behaviors. Think of Huntington’s disease, in which the devastating loss of motor function, memory, and impulse control are linked to a single gene, HTT. Think about the behavior of different dog breeds. The border collie’s intensity differs from the laid-back demeanor of the Labrador, and both of these tendencies differ from those of the happy yappy terrier. There is no doubt that these behavioral differences came about by selective breeding for specific traits, and that the basis for selective breeding is the heritability of those traits. Heritable traits, those that can be inherited, are affected by genes. No problem, but what about complex social behaviors?
Genes, Hormones, Monogamy, and Parental Care
We know that species differ in their mating strategies. Some species tend toward monogamy in that they show a strong preference for mating with a familiar partner, the parent of their own offspring. In these species, fathers tend to share the parental care of their own offspring, and these behaviors are often incompatible with high levels of aggressive competition. Other species tend toward promiscuity (multiple mating partners and no pair-bonds) and in these species, females tend to bear the burden of offspring care. We know quite a bit about hormonal control of these behaviors in certain species. Hormones are secreted from endocrine glands, and they act by binding to receptors. Hormone-receptor binding stimulates or inhibits the neural circuits that control behavior. In male prairie voles and marmoset monkeys, monogamy is linked to a number of hormones, two of which are oxytocin and vasopressin. Promiscuous species differ from monogamous species in the distribution of these receptors in the brain. One specific gene encodes the vasopressin V1A receptor, and monogamy in male voles is linked to the distribution of brain V1A receptors, which in turn is a consequence of the gene for this receptor. One form of the gene (a polymorphism) is linked with monogamy. How strong is the link between hormone receptor distribution and monogamy? In terms of their vasopressin and oxytocin receptors, monogamous marmoset monkeys look more like monogamous prairie voles than they look like promiscuous species of monkeys! Hormonal influences on monogamy and parental behaviors in birds and mammals are well accepted, and this line of research has provided insights into child neglect and abuse, postpartum depression, and autism.
Donna Maney and her students study song birds that are monogamous, but can be divided into two types, “dads or cads.” They study hormonally-mediated aggressive song and parental behavior in wild birds that form pair bonds with different levels of exclusivity. In biology, we say these species are “monogamous,” but this does not mean they don’t have sex with more than one partner. In these song birds, they all form pair bonds, but high levels of aggression and territoriality and low levels of offspring care are correlated with more “philandering,” that is, mating with multiple partners. In male birds, sex and aggressive behaviors are linked to hormones like testosterone from the testes and estradiol made from testosterone in the brain. As you will see, this model system affords unique advantages.
Two Morphs of White-throated Sparrow (Dads or Cads)
To link the evolution of behavior to specific genes, we need a snapshot of evolution in action, that is, we need two groups emerging within one population. Maney chose to study two different wild morphs within one population of white-throated sparrows (Zonotrichia albicollis). The morphs differ in their degree of aggressive song and parental care, as well as their propensity for multiple mating partners. As pictured at the top of this post, the tan-striped morph shows more parental behavior, more exclusive pair bonds, and less aggressive song, whereas the white-striped morph forms pair bonds, but also copulates freely with other birds. The white-striped males are less parental. Aggression can be easily measured by recording the species-typical song in response to that of an intruding male. Videos of the aggressive songs and display can be seen in the video here.
The two morphs also differ at chromosome 2, or ZAL2. Sparrows of the white-striped, aggressive morph all have at least one copy of a rearranged chromosome 2, ZAL2m, whereas the tan-striped sparrows never have this inverted chromosome. Donna Maney set out to study gene differences on this inverted chromosome that might explain differences in complex social behavior.
What’s Estrogen Got To Do With It?
In both morphs, the onset of aggressive, territorial song is correlated with increases in testosterone secreted from the testes during the breeding season (spring). Thus, you might suspect that the white-striped morph is more aggressive due to higher levels of testosterone. You would be wrong. When testosterone levels are equalized, the behavioral differences persist. There is something else going on. In the brains of sparrows and many song bird species, testosterone is converted to estradiol. Aggressive song is blocked by treatments that prevent conversion of testosterone to estradiol or by treatments that block estradiol binding to the estrogen receptor-alpha (ER-alpha) (reviewed by Kiran Soma). Receptors for estradiol, in particular ER-alpha, are located in brain areas involved in aggression, including the medial amygdala. Parental behavior is related to ER-alpha in other brain areas, including the medial preoptic area. The differences between the morphs might be related to differences in ER-alpha in the amygdala and preoptic area.
Just to remind you, Maney and colleagues knew that wild males of the more aggressive, white-striped morphs all have at least one copy of a rearranged copy of chromosome 2 (the rearranged chromosome is called ZAL2m). It turns out, the gene for ER-alpha, called ESR1, is located on this chromosome. Yes. Maney and her colleagues hypothesized that the rearrangement in the chromosome led to a change in ESR1 that led to elevated sensitivity to estradiol, and hence, higher levels of aggression and less parental behavior.
Indeed, Horton et al. found that the white-striped sparrows’ aggression was associated with a more efficient transcription of the gene, ESR1. That is, when the DNA is transcribed to messenger RNA, it occurred at a greater rate in the more aggressive, less parental, white-striped birds. More transcription might led to more translation, and hence more ER-alpha. This would be expected to render the white-striped birds more sensitive to estradiol’s effects on behavior.
Furthermore, Horton et al., found that in the white-throated morphs, territorial singing and ESR1 expression were higher in a region of the medial amygdala associated with aggression. Similarly, levels of nest provisioning were predicted by the level of ESR1 expression in the medial preoptic area. Thus, Maney’s group 1) linked a genetic change to a change in behavior, 2) linked a genetic change to a change in efficiency of gene transcription, 3) linked a change in gene expression in a particular brain area to a change in a particular behavior.
Together, these results are consistent with the idea that a genetic change in the gene for the estrogen receptor-alpha has led to the evolution of two different morphs of sparrow that differ in complex social behaviors. These experiments were done using wild birds from natural environments, not just laboratory animals. This and other work on this species was blogged by the awesome, Grrlscientist, at the Guardian. To the best of my knowledge, the Horton et al. article is the first such report in any vertebrate species.
It Takes All Kinds of Birds
Depending on your personal bias, you probably jump to the conclusion that one morph is better than the other, and one morph will win out. Exclusive pair bonds and low levels of aggression might result in more offspring if the offspring receive more parental care. The investment in parental care leads to a pay off in terms of number of reproductively successful offspring. On the other hand, aggressive, less parental birds can win larger territories and a greater abundance of resources (food and shelter). As this blog documents, the more energy, the greater the reproductive success. Read our latest review for more info on energy and reproduction. I wonder whether the frequency of the different morphs would change depending on the availability of energy in the environment. In any case, this means that in the white-stripe, “Don Draper-like” morph, greater investment in competition for resources might lead to more matings, greater fertility, and higher levels of long-term reproductive success. Maney tells us that these two morphs are not in competition, and probably not about to evolve into two separate species.
In reality, almost all white-throated sparrow breeding pairs consist of one individual with and one without the inverted ZAL2m chromosome. The females also differ in their level of parental investment. In other words, the tan-striped morph invariably mates with the white-striped morph, and the tan-striped male or tan-striped female takes up the slack at the nest. This increases the frequency of heterozygous individuals, and maintains the inverted chromosome ZAL2m in the population. Presumably, there is an evolutionary advantage to both the original version of chromosome 2 and the inverted chromosome ZAL2m, perhaps related to differential parental investment. It’s fascinating that the tan-striped males tend to mate with the more aggressive and territorial females and pick up the slack in the parenting department.
Maney and colleagues and their elegant experiments have shown that in white-throated sparrows, rearrangement of a specific gene, ESR1, is one of the genetic changes that underlies the emergence of two different, complementary life-history strategies.
In birds, voles, and monkeys, the behaviors are measured with precision, and these animals can’t deny, lie about, or exaggerate their sex behaviors. A number of studies have associated human monogamous/promiscuous and parental/nonparental tendencies with genetic polymorphisms, but it’s reasonable to wonder whether monogamy can be studied with any precision in people with such complicated sexuality. When it comes to sex, people are inhibited, shy, disingenuous, priggish, or boastful, rather than factual. Questions about human sexuality might have to wait until sex researchers get a hold of the data compiled by the NSA (that is, data compiled when the agents aren’t spying on their own love interests). Ah, yes. Therein lies a clue.
Well, if humans share anything in common with white-throated sparrows, it would surely be reflected in our musical archives…