Evolution of a Behavioral Character in a Sparrow Species

            Although the mutational study of behavioral characters was initiated by Seymour Benzer in the 1960’s, his study was concerned primarily with laboratory mutations of fruitflies and did not give much insight into the evolutionary mechanisms of behavioral characters in the wild. For this reason, many authors are now investigating this problem at the molecular level. Horton et al. (2014) recently published an interesting result with respect to the social behavior in the white-throated sparrow Zonotrichia albicollis.

In the white-throated sparrow there are two polymorphic phenotypes with respect to the color pattern of the head crown: (1) tan-striped (TS) and (2) white-striped (WS) (Fig. 1). The male WS phenotype is known to be more aggressive than the male TS with respect to territoriality and mate-finding. In song-birds, these behaviors are typically dependent on sex steroid during the breeding season. WS birds have higher plasma testosterone than the same sex TS birds. However, morph differences in behavior cannot be entirely explained by these hormones, because the differences persist even when plasma levels are experimentally equalized. Therefore, individual variation in steroid-dependent behavior may be better explained by neural sensitivity to the hormones, for example by variation in the distribution and abundance of steroid receptors (Horton et al., 2014).

  From Horton et al. (2014).

By the way, the WS and TS are associated with two inversion haplotypes of chromosome 2 (Thomas et al. 2008). That is, the genes controlling WS and TS are apparently located in the inverted segment of haplotypes ZAL2^m and ZAL2. However, because WS is dominant over TS and the frequency of ZAL2^m is relatively low, individuals can roughly be divided into two groups, WS (ZAL2^m/ZAL2,) and TS (ZAL2/ZAL2), genotype ZAL2^m/ZAL2^m, being practically absent. It has also been inferred that ZAL2^m was derived from ZAL2 about 2 million years ago by chromosomal inversion and therefore the polymorphism has existed for a long time. Note also that there is practically no recombination between two inverted chromosomes.

Horton et al. (2014) looked for steroid receptor genes in the inverted segment and found that the gene (ESR1) encoding estrogen receptor α (ERα) is located in the inverted segment and that the two proteins encoded by the ESR1 genes from the WS and TS phenotypes showed one amino acid difference but this difference did not affect the gene expression pattern appreciably. They then hypothesized that the phenotypic difference between WS and TS is caused by the difference in the gene regulatory region of the gene. In fact, when the binding sites of transcription factors in the cis-regulatory region upstream of the ESR1 gene were examined by a computer program, there was considerable difference between the WS and TS haplotypes (Fig. 2A).

 From Horton et al. (2014).

However, to prove that this difference is indeed responsible for the behavioral difference, it was necessary to show that the expression level of the ESR1 gene is higher in haplotype ZAL2^m than in ZAL2. For this purpose, Horton et al. used several molecular techniques such as the luciferase reporter method with HeLa cells and radioimmunoassay. Their results showed that the expression level of the ESR1 gene is about 1.5 times higher in haplotype ZAL2^m than in ZAL2 (Fig. 2B,C).

This finding indicates that the difference in expression level of a single major gene generates a clear phenotypic difference, which in turn affects an important behavioral character. At the present time, this type of data is rare, but it is possible that many behavioral characters are controlled by similar molecular mechanisms, and it is desirable that more studies will be conducted in the future. In practice, behavioral characters are generally controlled by many genes, and eventually we may be able to understand the molecular basis of the characters. Yet, the basic principle of gene expression could be simpler than our intuition suggests as in the case of the above example. In their “significance” statement, Horton et al. write:

In this series of studies, we provide a rare illustration of how a chromosomal polymorphism has affected overt social behavior in a vertebrate. White-throated sparrows occur in two alternative phenotypes, or morphs, distinguished by a chromosomal rearrangement. That the morphs differ in territorial and parental behavior has been known for decades, but how the rearrangement affects behavior is not understood. Here we show that genetic differentiation between the morphs affects the transcription of a gene well known to be involved in social behavior. We then show that in a free-living population, the neural expression of this gene predicts both territorial and parental behavior. We hypothesize that this mechanism has played a causal role in the evolution of alternative life-history strategies.