The evolutionary loss of a badge of status alters male competition in three-spine stickleback

Abstract

The evolutionary loss of sexual signals is taxonomically widespread and quite common. These signals are often important not only in mate choice but also in male competition for territories and females; yet, male competition has rarely been investigated in the context of signal loss. We asked whether the loss of red throat color in three-spine stickleback (Gasterosteus aculeatus), an ancestral signal important in both male competition and mate choice, is accompanied by changes to intrasexual selection. Several freshwater stickleback populations have lost the red throat, and instead develop black breeding coloration. Previous work demonstrated that sensory drive is likely responsible. We conducted trials that mimic contact between ancestral (red) and derived (black) types during territory and nest establishment under conditions mimicking the 2 water color environments (clear and red-shifted, respectively) where they are found. We found that the allocation of competition behaviors depends on male breeding color, but not water color or the interaction of the 2. Although the total number of aggressive behaviors did not vary between color types, black males directed more aggression toward red males. Assessing each male competition behavior separately revealed that this pattern was largely driven by black fish biasing "charges" toward opposite type males. Agonistic behavior between types may strengthen divergence in resource or habitat use between populations of males with and without the ancestral sexual signal.

Phenotypic divergence among threespine stickleback that differ in nuptial coloration

“…Recent work in red and black stickleback from Washington State similarly supports a role for sexual selection in the divergence of red and black stickleback, albeit through changes in male competition behavior, rather than female preferences (Tinghitella et al, 2015;Tinghitella, Lehto, et al, 2018). In simulated secondary contact in the laboratory, females from populations containing only red or only K E Y W O R D S color morph, Gasterosteus aculeatus, phenotypic divergence, threespine stickleback black males retain their ancestral preference for the red mating signal (McKinnon, 1995) and prefer to interact with red males (Tinghitella et al, 2015). Though there is no evidence of assortative mating, male competition for territories, which occurs prior to female mate choice in the breeding season, may be an important isolating mechanism in this system; in Washington, black males bias their aggression toward red males, so red males receive more aggression overall than black males.…”

Male competition drives song divergence along an ecological gradient in an avian ring species

“…Moreover, there is increasing evidence for a direct role of male competition in diversification: color divergence in darters ( Etheostoma ) has been attributed to male competition rather than female choice (Martin and Mendelson ), and male competition based on throat color may enhance ecological divergence in sticklebacks ( Gasterosteus , Tinghitella et al. ).…”

“…However, studies from a variety of taxa show that aggressive behavior and territorial defense vary geographically (Newman et al 2006;Apfelbeck and Goymann 2011;Bastianelli et al 2015), with ecological factors such as population density (Gosden and Svensson 2008), resource distribution (Taff et al 2013), sex ratio (Kokko and Rankin 2006), and breeding synchrony (Thusius et al 2001), and may be heritable targets of selection (Sih et al 2004). Moreover, there is increasing evidence for a direct role of male competition in diversification: color divergence in darters (Etheostoma) has been attributed to male competition rather than female choice (Martin and Mendelson 2016), and male competition based on throat color may enhance ecological divergence in sticklebacks (Gasterosteus, Tinghitella et al 2015).…”

Opsin expression predicts male nuptial color in threespine stickleback

“…Bolnick et al (2016) provided evidence for negative frequency-dependent selection via male-male competition in two lake populations of stickleback that differ in male nuptial color. In lakes where native males are predominantly red-throated, red-throated models were attacked more frequently and with a higher intensity, while the opposite was the case for lakes with melanic males (Bolnick et al 2016; but see Tinghitella, Lehto, & Minter, 2015). These results were also modulated within lakes by depth, a proxy for optical environment (Bolnick et al 2016;Brock et al, 2017a;Brock, Bolnick, & Cummings, 2017b).…”

“…In lakes where native males are predominantly red‐throated, red‐throated models were attacked more frequently and with a higher intensity, while the opposite was the case for lakes with melanic males (Bolnick et al. ; but see Tinghitella, Lehto, & Minter, ). These results were also modulated within lakes by depth, a proxy for optical environment (Bolnick et al.…”