Social aggression mediated via kin selection and ecological competition in the Amazon molly, Poecilia formosa

The maintenance of sexual reproduction is still a largely unresolved question in evolutionary biology, and one of the most puzzling aspects of this is the co-existence of sexual and asexual species. This often leads to widespread niche overlap, posing an interesting challenge to the Competitive Exclusion Principle. Despite this, there seems to be something preventing either the sexuals or asexuals from outcompeting the other. I investigated this using the clonal fish, the Amazon molly (Poecilia formosa). Females produce daughters that are genetically identical to themselves and each other, and are sexual parasites of their parental species, the sailfin molly (P. latipinna) and the Atlantic molly (P. mexicana). They overlap and compete in many aspects of their ecological niche, behavioral, and life history parameters. The ‘behavioral regulation hypothesis’ predicts that the maintenance of this species complex is driven by adaptive male mate choice. However, little attention has been given to counter-adaptations that may allow Amazon females to thwart male mate choice. One of the most likely means of circumventing male choice is aggression towards the preferred sexual females. Here, I investigated two questions: 1) How costly is female-female aggressive behaviors in Amazon mollies in comparison to sailfin females, and 2) How does the social environment help regulate aggression in Amazon females (i.e., kin selection). First, I found that Amazon females were on average more aggressive over time when compared to their sexual hosts, sailfin molly females. Amazon females, however, incurred a higher cost of being aggressive. Aggressor females of this species had a lower body fat content than their conspecific recipients. By contrast, sailfin females showed no differentiation between aggressors and recipients. Secondly, Amazon mollies have the ability to distinguish between different clonal lineages: clonal females prefer genetically identical, clonal sisters to slightly different clones. Intriguingly, they do this using multiple sensory modalities, including visual and/or chemical cues. In natural water, wild caught females preferred clonal sisters when chemical information was available, while the preference using visual information was non-existent. Most importantly, however, they scale their aggressive behaviors according to the relatedness to other females: they are more aggressive to non-related clones. In conclusion, female competition can be quantitatively measured and that these aggressive behaviors are costly to perform. I demonstrate that even in species with very small genetic differences between individuals, kin selection can be adaptive. Indeed, even minute differences in relatedness (extremely close kin are favored over very close kin) can provide enough substrate for the evolution of kin recognition. Their discriminatory abilities and regulation of behavior provides a powerful example of natural selection in species with limited genetic diversity

Sexual harassment in live-bearing fishes (Poeciliidae): comparing courting and noncourting species

Sexual harassment by males has been reported from several live-bearing fishes (Poeciliidae) and has been shown to inflict costs on females. For example, poeciliid females have reduced feeding opportunities when accompanied by a male because females dedicate attention to avoiding male copulation attempts. Poeciliid species differ considerably in male mating behavior, such as the presence or absence of courtship. Courting males display in front of the females, but males attempting to sneak-copulate approach females from behind, that is, in the blind portion of their visual field, and force copulations, which can be viewed as a male persistence trait. We predicted that poeciliid females need to be more vigilant in the presence of noncourting males, and costs of harassment by noncourting males might be stronger. In a comparative approach we examined the costs of male sexual harassment for females as reduced feeding time in 9 species of live-bearing fishes, including courting (Poecilia latipinna, Poecilia reticulata, Xiphophorus cortezi, Xiphophorus variatus) and noncourting species (Poecilia mexicana [surface- and cave-dwelling form], Poecilia orri, Gambusia affinis, Gambusia geiseri, Heterandria formosa). In all species examined except for the cave form of P. mexicana, focal females spent significantly less time feeding in the presence of a male than when together with another female. The time females spent feeding was found to significantly decline with increasing male mating activity (sum of all sexual behaviors), but there was no support for the idea that females would spend more time feeding in the presence of courting males compared with noncourting one

Casanovas are liars : behavioral syndromes, sperm competition risk, and the evolution of deceptive male mating behavior in live-bearing fishes [version 2; referees: 2 approved, 1 approved with reservations]

Male reproductive biology can by characterized through competition over mates as well as mate choice. Multiple mating and male mate choice copying, especially in internally fertilizing species, set the stage for increased sperm competition, i.e., sperm of two or more males can compete for fertilization of the female’s ova. In the internally fertilizing fish Poecilia mexicana, males respond to the presence of rivals with reduced expression of mating preferences (audience effect), thereby lowering the risk of by-standing rivals copying their mate choice. Also, males interact initially more with a non-preferred female when observed by a rival, which has been interpreted in previous studies as a strategy to mislead rivals, again reducing sperm competition risk (SCR). Nevertheless, species might differ consistently in their expression of aggressive and reproductive behaviors, possibly due to varying levels of SCR. In the current study, we present a unique data set comprising ten poeciliid species (in two cases including multiple populations) and ask whether species can be characterized through consistent differences in the expression of aggression, sexual activity and changes in mate choice under increased SCR. We found consistent species-specific differences in aggressive behavior, sexual activity as well as in the level of misleading behavior, while decreased preference expression under increased SCR was a general feature of all but one species examined. Furthermore, mean sexual activity correlated positively with the occurrence of potentially misleading behavior. An alternative explanation for audience effects would be that males attempt to avoid aggressive encounters, which would predict stronger audience effects in more aggressive species. We demonstrate a positive correlation between mean aggressiveness and sexual activity (suggesting a hormonal link as a mechanistic explanation), but did not detect a correlation between aggressiveness and audience effects. Suites of correlated behavioral tendencies are termed behavioral syndromes, and our present study provides correlational evidence for the evolutionary significance of SCR in shaping a behavioral syndrome at the species level across poeciliid taxa

Casanovas are liars: behavioral syndromes, sperm competition risk, and the evolution of deceptive male mating behavior in live-bearing fishes

Male reproductive biology can by characterized through competition over mates as well as mate choice. Multiple mating and male mate choice copying, especially in internally fertilizing species, set the stage for increased sperm competition, i.e., sperm of two or more males can compete for fertilization of the female’s ova. In the internally fertilizing fish Poecilia mexicana, males respond to the presence of rivals with reduced expression of mating preferences (audience effect), thereby lowering the risk of by-standing rivals copying their mate choice. Also, males interact initially more with a non-preferred female when observed by a rival, which has been interpreted in previous studies as a strategy to mislead rivals, again reducing sperm competition risk (SCR). Nevertheless, species might differ consistently in their expression of aggressive and reproductive behaviors, possibly due to varying levels of SCR. In the current study, we present a unique data set comprising ten poeciliid species (in two cases including multiple populations) and ask whether species can be characterized through consistent differences in the expression of aggression, sexual activity and changes in mate choice under increased SCR. We found consistent species-specific differences in aggressive behavior, sexual activity as well as in the level of misleading behavior, while decreased preference expression under increased SCR was a general feature of all but one species examined. Furthermore, mean sexual activity correlated positively with the occurrence of potentially misleading behavior. An alternative explanation for audience effects would be that males attempt to avoid aggressive encounters, which would predict stronger audience effects in more aggressive species. We demonstrate a positive correlation between mean aggressiveness and sexual activity (suggesting a hormonal link as a mechanistic explanation), but did not detect a correlation between aggressiveness and audience effects. Suites of correlated behavioral tendencies are termed behavioral syndromes, and our present study provides correlational evidence for the evolutionary significance of SCR in shaping a behavioral syndrome at the species level across poeciliid taxa

Kin recognition in a clonal fish, Poecilia formosa

Relatedness strongly influences social behaviors in a wide variety of species. For most species, the highest typical degree of relatedness is between full siblings with 50% shared genes. However, this is poorly understood in species with unusually high relatedness between individuals: clonal organisms. Although there has been some investigation into clonal invertebrates and yeast, nothing is known about kin selection in clonal vertebrates. We show that a clonal fish, the Amazon molly (Poecilia formosa), can distinguish between different clonal lineages, associating with genetically identical, sister clones, and use multiple sensory modalities. Also, they scale their aggressive behaviors according to the relatedness to other females: they are more aggressive to non-related clones. Our results demonstrate that even in species with very small genetic differences between individuals, kin recognition can be adaptive. Their discriminatory abilities and regulation of costly behaviors provides a powerful example of natural selection in species with limited genetic diversity.Funding was provided by an Adams Memorial Scholarship, Robberson Research Grant, Graduate Student Senate Research Grant, L.G. Hill Award, Eddie Carol Smith Scholarship, GAANN fellowship (AMM), and an Alexander von Humboldt Foundation Research Award (IS).Ye

Data from: Host species of a sexual-parasite do not differentiate between clones of Amazon mollies

A major mechanism of pre-zygotic isolation is the ability for individuals to recognize conspecifics. In gynogenetic species complexes, the sexual host species occur in syntopy with the unisexual species that relies on the sexuals’ sperm for reproduction, which provide an excellent opportunity for the evolution of fine-tuned species recognition capabilities. Here, we examined if males and females from both parental species (sailfin molly, Poecilia latipinna, and Atlantic molly, P. mexicana) can distinguish between different clonal lineages of the hybrid, all-female Amazon molly (P. formosa). Both males and females were presented with the choice of two different pairings of Amazon mollies: 1) a sympatric female and an allopatric female; and 2) two sympatric females. We found that neither males nor females of sailfin or Atlantic mollies show a preference for a clone type. These results suggest that either the parental species do not have the ability to recognize different Amazon molly clones or they recognize but do not have a preference for a specific Amazon molly clone

Data from: Host species of a sexual-parasite do not differentiate between clones of Amazon mollies

A major mechanism of pre-zygotic isolation is the ability for individuals to recognize conspecifics. In gynogenetic species complexes, the sexual host species occur in syntopy with the unisexual species that relies on the sexuals’ sperm for reproduction, which provide an excellent opportunity for the evolution of fine-tuned species recognition capabilities. Here, we examined if males and females from both parental species (sailfin molly, Poecilia latipinna, and Atlantic molly, P. mexicana) can distinguish between different clonal lineages of the hybrid, all-female Amazon molly (P. formosa). Both males and females were presented with the choice of two different pairings of Amazon mollies: 1) a sympatric female and an allopatric female; and 2) two sympatric females. We found that neither males nor females of sailfin or Atlantic mollies show a preference for a clone type. These results suggest that either the parental species do not have the ability to recognize different Amazon molly clones or they recognize but do not have a preference for a specific Amazon molly clone

Male clonal recog data- Dryad

Raw data for male and female preferences in Poecilia latipinna and Poecilia formos

Casanovas are liars : behavioral syndromes, sperm competition risk, and the evolution of deceptive male mating behavior in live-bearing fishes [version 3; referees: 3 approved]

Male reproductive biology can by characterized through competition over mates as well as mate choice. Multiple mating and male mate choice copying, especially in internally fertilizing species, set the stage for increased sperm competition, i.e., sperm of two or more males can compete for fertilization of the female’s ova. In the internally fertilizing fish Poecilia mexicana, males respond to the presence of rivals with reduced expression of mating preferences (audience effect), thereby lowering the risk of by-standing rivals copying their mate choice. Also, males interact initially more with a non-preferred female when observed by a rival, which has been interpreted in previous studies as a strategy to mislead rivals, again reducing sperm competition risk (SCR). Nevertheless, species might differ consistently in their expression of aggressive and reproductive behaviors, possibly due to varying levels of SCR. In the current study, we present a unique data set comprising ten poeciliid species (in two cases including multiple populations) and ask whether species can be characterized through consistent differences in the expression of aggression, sexual activity and changes in mate choice under increased SCR. We found consistent species-specific differences in aggressive behavior, sexual activity as well as in the level of misleading behavior, while decreased preference expression under increased SCR was a general feature of all but one species examined. Furthermore, mean sexual activity correlated positively with the occurrence of potentially misleading behavior. An alternative explanation for audience effects would be that males attempt to avoid aggressive encounters, which would predict stronger audience effects in more aggressive species. We demonstrate a positive correlation between mean aggressiveness and sexual activity (suggesting a hormonal link as a mechanistic explanation), but did not detect a correlation between aggressiveness and audience effects. Suites of correlated behavioral tendencies are termed behavioral syndromes, and our present study provides correlational evidence for the evolutionary significance of SCR in shaping a behavioral syndrome at the species level across poeciliid tax

Preferences for Familiarity.

<p>The average ± SE for female preferences of clonal sisters and non-sisters was not due to familiarity. In each experiment, 15 females were given a choice between a familiar clonal sister (red), an unfamiliar clonal sister (yellow), or an unfamiliar non-sister (blue) after a 10-month isolation period from clonal sisters. <b>A.</b> Females from Comal Spring, TX, familiar clonal sisters and unfamiliar non-sisters, <i>t</i>₍₁₅₎ = 5.213, <i>p</i><0.0001; <b>B.</b> Unfamiliar clonal sisters and unfamiliar non-sisters, <i>t</i>₍₁₅₎ = 3.362, <i>p</i> = 0.005; <b>C.</b> Familiar clonal sisters and unfamiliar clonal sisters, <i>t</i>₍₁₄₎ = 2.966, <i>p</i> = 0.011. Females maintain the preference for clonal sisters (regardless of familiarity) and prefer familiar clonal sisters to unfamiliar clonal sisters.</p