Parental care, mating dynamics and life history co‐evolve. Understanding the diversity of reproductive patterns found in nature is a major focus of evolutionary ecology research. Previous research suggests that the origin of parental care of eggs will be favoured when egg and adult death rates and juvenile survival are relatively high. However, the previous research that explored the link between care and life history did not account for among‐species variation in mating dynamics. As mating dynamics are generally expected to influence care, we explore, theoretically, the life‐history conditions (stage‐specific rates of maturation and survival) that favour parental care across three mating scenarios: reproductive rate (1) is unaffected by males (assuming that some males are present), (2) increases as male abundance increases or (3) decreases as male abundance increases. Across scenarios, all forms of care were most strongly favoured when egg and adult death rates, juvenile survival and female egg maturation rates were relatively high. When reproductive rate was unaffected by male abundance or increased as male abundance increased, as we might expect in systems in which females are mate‐limited, all forms of care were most strongly favoured when male egg maturation rate (i.e. the rate at which male eggs develop, mature and hatch) was moderate or high. When greater male abundance inhibited reproduction, which might occur in systems with intense male–male competition, all forms of care were most strongly favoured when male egg maturation rate was low‐to‐moderate. These results suggest that life history affects the evolution of parental care, and sex‐specific life history can interact with mating dynamics to influence the origin of care.
Parental care is essential to offspring survival in many species. Understanding why males of some species provide care, whereas others do not, has received substantial attention. Previous research has found that sexual selection can favor paternal care, yet we still do not fully understand why sexual selection favors male care in some species but not others. It is also unclear when paternal care versus other preferred male trait(s) will be favored by sexual selection. We hypothesize that sexual selection can interact with basic life history to influence the conditions under which paternal care and/or another preferred male trait will be favored by sexual selection. We used a mathematical approach in which males alone provide parental care and exhibit a non‐care trait that is preferred in mate choice. Using this approach, we demonstrate that life‐history characteristics (stage‐specific mortality, fertilization success, gamete numbers) can interact with sexual selection to influence the evolution of paternal care and/or a preferred non‐care trait. In particular, whether (1) adult mortality, egg mortality, and fertilization success are high versus low and (2) a tradeoff exists between paternal care and a non‐care preferred trait will influence whether selection most strongly favors additional paternal care or a non‐care preferred trait. In general, we would expect strong selection for more male care when it is preferred in mate choice. In some cases, mate preferences for paternal care can inhibit selection for a preferred non‐care trait. Mate preferences for paternal care can also broaden the life‐history conditions under which we would expect the elaboration of male care to occur.
more » « less- PAR ID:
- 10535157
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology and Evolution
- Volume:
- 14
- Issue:
- 8
- ISSN:
- 2045-7758
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Males in many species have elaborated sexual traits that females strongly prefer, and these traits often conspicuously differ among species. How novel preferences and traits originate, however, is a challenging evolutionary problem because the initial appearance of only the female preference or only the male trait should reduce the ability to find a suitable mate, which could reduce fitness for individuals possessing those novel alleles. Here, we present a hypothesis for how novel preferences, as well as the novel male traits that females prefer, can originate, be favoured and spread in polyandrous species. Novel preference mutations can arise as ‘veiled preferences’ that are not expressed when the corresponding male trait is not present in the population, allowing preferences to be hidden from selection, and thus persist. In those cases when a male trait is present, veiled preferences provide a selective advantage, and females disproportionately produce offspring from preferred males through either mate choice or cryptic female choice. This tips the fitness advantage for novel males, allowing both preference and trait to spread, and limiting selection against them in the absence of the corresponding trait or preference.
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BACKGROUND Charles Darwin’s Descent of Man, and Selection in Relation to Sex tackled the two main controversies arising from the Origin of Species: the evolution of humans from animal ancestors and the evolution of sexual ornaments. Most of the book focuses on the latter, Darwin’s theory of sexual selection. Research since supports his conjecture that songs, perfumes, and intricate dances evolve because they help secure mating partners. Evidence is overwhelming for a primary role of both male and female mate choice in sexual selection—not only through premating courtship but also through intimate interactions during and long after mating. But what makes one prospective mate more enticing than another? Darwin, shaped by misogyny and sexual prudery, invoked a “taste for the beautiful” without speculating on the origin of the “taste.” How to explain when the “final marriage ceremony” is between two rams? What of oral sex in bats, cloacal rubbing in bonobos, or the sexual spectrum in humans, all observable in Darwin’s time? By explaining desire through the lens of those male traits that caught his eyes and those of his gender and culture, Darwin elided these data in his theory of sexual evolution. Work since Darwin has focused on how traits and preferences coevolve. Preferences can evolve even if attractive signals only predict offspring attractiveness, but most attention has gone to the intuitive but tenuous premise that mating with gorgeous partners yields vigorous offspring. By focusing on those aspects of mating preferences that coevolve with male traits, many of Darwin’s influential followers have followed the same narrow path. The sexual selection debate in the 1980s was framed as “good genes versus runaway”: Do preferences coevolve with traits because traits predict genetic benefits, or simply because they are beautiful? To the broader world this is still the conversation. ADVANCES Even as they evolve toward ever-more-beautiful signals and healthier offspring, mate-choice mechanisms and courter traits are locked in an arms race of coercion and resistance, persuasion and skepticism. Traits favored by sexual selection often do so at the expense of chooser fitness, creating sexual conflict. Choosers then evolve preferences in response to the costs imposed by courters. Often, though, the current traits of courters tell us little about how preferences arise. Sensory systems are often tuned to nonsexual cues like food, favoring mating signals resembling those cues. And preferences can emerge simply from selection on choosing conspecifics. Sexual selection can therefore arise from chooser biases that have nothing to do with ornaments. Choice may occur before mating, as Darwin emphasized, but individuals mate multiple times and bias fertilization and offspring care toward favored partners. Mate choice can thus occur in myriad ways after mating, through behavioral, morphological, and physiological mechanisms. Like other biological traits, mating preferences vary among individuals and species along multiple dimensions. Some of this is likely adaptive, as different individuals will have different optimal mates. Indeed, mate choice may be more about choosing compatible partners than picking the “best” mate in the absolute sense. Compatibility-based choice can drive or reinforce genetic divergence and lead to speciation. The mechanisms underlying the “taste for the beautiful” determine whether mate choice accelerates or inhibits reproductive isolation. If preferences are learned from parents, or covary with ecological differences like the sensory environment, then choice can promote genetic divergence. If everyone shares preferences for attractive ornaments, then choice promotes gene flow between lineages. OUTLOOK Two major trends continue to shift the emphasis away from male “beauty” and toward how and why individuals make sexual choices. The first integrates neuroscience, genomics, and physiology. We need not limit ourselves to the feathers and dances that dazzled Darwin, which gives us a vastly richer picture of mate choice. The second is that despite persistent structural inequities in academia, a broader range of people study a broader range of questions. This new focus confirms Darwin’s insight that mate choice makes a primary contribution to sexual selection, but suggests that sexual selection is often tangential to mate choice. This conclusion challenges a persistent belief with sinister roots, whereby mate choice is all about male ornaments. Under this view, females evolve to prefer handsome males who provide healthy offspring, or alternatively, to express flighty whims for arbitrary traits. But mate-choice mechanisms also evolve for a host of other reasons Understanding mate choice mechanisms is key to understanding how sexual decisions underlie speciation and adaptation to environmental change. New theory and technology allow us to explicitly connect decision-making mechanisms with their evolutionary consequences. A century and a half after Darwin, we can shift our focus to females and males as choosers, rather than the gaudy by-products of mate choice. Mate choice mechanisms across domains of life. Sensory periphery for stimulus detection (yellow), brain for perceptual integration and evaluation (orange), and reproductive structures for postmating choice among pollen or sperm (teal). ILLUSTRATION: KELLIE HOLOSKI/ SCIENCEmore » « less
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Patricelli, Gail L. (Ed.)more » « less
Sexual selection by mate choice is a powerful force that can lead to evolutionary change, and models of why females choose particular mates are central to understanding its effects. Predominant mate choice theories assume preferences are determined solely by genetic inheritance, an assumption still lacking widespread support. Moreover, preferences often vary among individuals or populations, fail to correspond with conspicuous male traits, or change with context, patterns not predicted by dominant models. Here, we propose a new model that explains this mate choice complexity with one general hypothesized mechanism, “Inferred Attractiveness.” In this model, females acquire mating preferences by observing others’ choices and use context-dependent information to infer which traits are attractive. They learn to prefer the feature of a chosen male that most distinguishes him from other available males. Over generations, this process produces repeated population-level switches in preference and maintains male trait variation. When viability selection is strong, Inferred Attractiveness produces population-wide adaptive preferences superficially resembling “good genes.” However, it results in widespread preference variation or nonadaptive preferences under other predictable circumstances. By casting the female brain as the central selective agent, Inferred Attractiveness captures novel and dynamic aspects of sexual selection and reconciles inconsistencies between mate choice theory and observed behavior.
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Abstract Investigating how intrasexual competition and intersexual mate choice act within a system is crucial to understanding the maintenance and diversity of sexually-dimorphic traits. These two processes can act in concert by selecting for the same trait, or in opposition by selecting for different extremes of the same trait; they can also act on different traits, potentially increasing trait complexity. We asked whether male–male competition and female mate choice act on the same male traits using Trinidadian guppies, which exhibit sexual size dimorphism and male-limited color patterns consisting of different colors arranged along the body and fins. We used behavioral assays to assess the relationship between color and competitive success and then compared our results to the plethora of data on female choice and color in our study population. Males initiated more contests if they were larger than their competitor. Males won contests more often if they had more black coloration than their competitor, and the effect of black was stronger when males had less orange than their competitor. Additionally, males won more often if they had either more structural color (iridescence) and more orange, or less structural color and less orange than their competitor, suggesting multiple combinations of color traits predict success. Females from our study population exhibit a strong preference for more orange coloration. Thus, traits favored in male contests differ from those favored by intersexual selection in this population. These results suggest that inter- and intrasexual selection, when acting concurrently, can promote increased complexity of sexually selected traits.
