Neuromotor and neuroendocrine mechanisms underlying display behavior

Sexual selection favors the evolution of increasingly complex behavioral traits used to court mates and fight off rivals. When these displays are physical in nature, display performance requires coordinated action of brain, hormones, and skeletal muscles. We study these mechanisms of behavior in a number of ways.

 

1. Morphological and physiological adaptations for physical display behavior

When sexual selection favors increasingly elaborate physical displays, some of these gestures are so extreme that they are reflected in morphological innovations. We study the morphology that underlies display behavior in manakins, a family of lekking tropical birds. Many manakin species perform downright acrobatic displays, which are supported by modifications of both skeleton and muscles.

Flattened bones in wings that go "snap"

Manakins in the genus Manacus, like the golden-collared manakin (Manacus vitellinus), use a courtship behavior called the wing-snap, produced by rapidly hitting the wrists together. In studying how morphology influences behavior, we found that these species also have a radius that is both flattened and solidified relative to other species. 

high-speed muscleS specialized for displaying

Wing-snap gestures rely on fast muscle contraction as well. In fact, we've found that the golden collared manakin can contract its scapulohumeralis wing muscle faster than any other tetrapod in the world, which allows it to hit its wings together over 100 times per second. We are currently trying to understand how this remarkable shift in physiological performance was able to come about.

Mvit_Anatomy.png
 
 Juvenile male manakins like the red-capped manakin ( Ceratopipra mentalis ), above, start practicing their wing-snap displays before they've achieved their definitive (adult) plumage.

Juvenile male manakins like the red-capped manakin (Ceratopipra mentalis), above, start practicing their wing-snap displays before they've achieved their definitive (adult) plumage.

 

Read more: 

Friscia A, Sanin GD, Lindsay WR, Day LB, Schlinger BA, Tan J, and MJ Fuxjager. 2016. Adaptive evolution of a derived radius morphology in manakins (Aves, Pipridae) to support acrobatic display behavior. Journal of Morphology. 277: 766-775. [pdf]

Fuxjager MJ, Goller F, Dirske A, Sanin GD, and S Garcia. 2016. Select forelimb muscles have evolved superfast contractile speed to support acrobatic social displays. eLife 5:e13544. [pdf]

2. Tissue-specific steroid hormone action

How are the musculoskeletal and nervous system specialized to facilitate the production of highly physical display behavior? For the male animals that display, we find that the answer largely lies in steroid hormone action. But while many other researchers focus on the effects of the hormone alone (i.e. changes in circulating testosterone levels), we study the potent downstream and peripheral mechanisms by which androgens support physical displays.

Androgens enhance motor performance

Androgens are sex steroid hormones that regulate an astounding variety of animal traits-- including muscle performance involved in producing display behavior. This is because androgenic receptor (AR), which is bound by multiple steroid hormones, is a transcription factor and therefore alters local gene expression. In manakins, for example, wing muscle AR activity is associated with increased expression of genes associated with calcium trafficking and muscle hypertrophy, both of which enhance muscle contraction.

We study how this works in birds like the golden-collared manakin, where we have found that wing-snap display behavior is androgen-dependent. Even more, this behavior appears to be regulated by peripheral (i.e. muscle tissue-specific) action of androgenic receptor (AR), and suppressing AR activity impedes an individual's ability to display. 

the power of Steroidogenic enzymes

While most people are familiar with the hormones testosterone (T) and estrogen (E), these are only two components of a complex steroid pathway. Steroidogenic enzymes are responsible for synthesizing downstream steroid metabolites like dihydrotestosterone (DHT), which is a much more potent activator of the AR transcription factor than T alone. Therefore, another mechanism to alter display behavior lies in modifying enzymatic activity. We have previously discovered that manakins express more of the T-inactivating enzyme 5ß-reductasein in both the central nervous system and skeletal muscle, when compared to zebra finches that do not produce physical displays. This suggests that inhibiting activity of less potent steroids may help further enhance muscle performance in species that produce physical displays.

Read more:

Fuxjager MJ, Lee J, Chan T, Bahn J, Chew J, Xiao X, and BA Schlinger. 2016. Hormones, genes and athleticism: effect of androgens on the avian muscular transcriptome. Molecular Endocrinology. 30: 254-271.  [pdf]

Fuxjager MJ, Schuppe ER, Hoang J, Chew J, Shah M, and Schlinger BA. 2016. Expression of 5α- and 5β-reductase in spinal cord and muscle of birds with different courtship repertoires. Frontiers in Zoology. 13:25.  [pdf]

Fuxjager MJ, Eaton J, Lindsay WR, Salwiczek LH, Rensel MA, Barske J, Sorenson L, Day LB, and BA Schlinger. 2015. Evolutionary patterns of adaptive acrobatics and physical performance predict expression profiles of androgen receptor – but not estrogen receptor – in the forelimb musculature. Functional Ecology. 29: 1197-1208. [pdf]