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1.
J Evol Biol ; 36(11): 1609-1617, 2023 11.
Article in English | MEDLINE | ID: mdl-37885146

ABSTRACT

Divergence of sexual signals between populations can lead to speciation, yet opportunities to study the immediate aftermath of novel signal evolution are rare. The recent emergence and spread of a new mating song, purring, in Hawaiian populations of the Pacific field cricket (Teleogryllus oceanicus) allows us to investigate population divergence soon after the origin of a new signal. Male crickets produce songs with specialized wing structures to attract mates from afar (calling) and entice them to mate when found (courtship). However, in Hawaii, these songs also attract an eavesdropping parasitoid fly (Ormia ochracea) that kills singing males. The novel purring song, produced with heavily modified wing morphology, attracts female crickets but not the parasitoid fly, acting as a solution to this conflict between natural and sexual selection. We've recently observed increasing numbers of purring males across Hawaii. In this integrative field study, we investigated the distribution of purring and the proportion of purring males relative to other morphs in six populations on four islands and compared a suite of phenotypic traits (wing morphology, calling song and courtship song) that make up this novel signal across populations of purring males. We show that purring is found in varying proportions across five, and is locally dominant in four, Hawaiian populations. We also show that calling songs, courtship songs and wing morphology of purring males differ geographically. Our findings demonstrate the rapid pace of evolution in island populations and provide insights into the emergence and divergence of new sexual signals over time.


Subject(s)
Gryllidae , Animals , Male , Female , Gryllidae/genetics , Sexual Behavior, Animal , Biological Evolution , Vocalization, Animal , Hawaii
2.
J Evol Biol ; 35(7): 934-947, 2022 07.
Article in English | MEDLINE | ID: mdl-35716364

ABSTRACT

Sexual signals are shaped by their intended and unintended receivers as well as the signalling environment. This interplay between sexual and natural selection can lead to divergence in signals in heterogeneous environments. Yet, the extent to which gene flow is restricted when signalling phenotypes vary across environments and over what spatial scales remains an outstanding question. In this study, we quantify gene flow between two colour morphs, red and black, of freshwater threespine stickleback fish (Gasterosteus aculeatus). We capitalize on the very recent divergence of signalling phenotypes in this system to characterize within-species and among-morph genetic variation and to test for levels of gene flow between colour morphs in Oregon and Washington. Despite limited evidence for assortative mating between allopatric red and black populations, we found that black populations are genetically distinct from nearby red populations and that the black morph appears to have evolved independently at least twice in Oregon and Washington. Surprisingly, we uncovered a group of stickleback in one small coastal stream, Connor Creek, which is genetically and morphologically distinct from the red and black colour morphs and from marine stickleback. Historically, both colour morphs have coexisted in this location and sometimes hybridized, raising new questions about the origins and history of these fish, which were first described as anadromous-black hybrids >50 years ago. Understanding how genetic variation is currently partitioned within and among populations and colour morphs in this system should prompt future studies to assess the relative roles of habitat, ecological and pre- and post-reproductive barriers in the genetic divergence and phenotypic patterns we observe in nature.


Subject(s)
Smegmamorpha , Animals , Ecosystem , Fishes , Gene Flow , Genetic Drift , Selection, Genetic , Smegmamorpha/anatomy & histology , Smegmamorpha/genetics
3.
Biol Lett ; 17(2): 20200733, 2021 02.
Article in English | MEDLINE | ID: mdl-33529546

ABSTRACT

The diversity of signalling traits within and across taxa is vast and striking, prompting us to consider how novelty evolves in the context of animal communication. Sexual selection contributes to diversification, and here we endeavour to understand the initial conditions that facilitate the maintenance or elimination of new sexual signals and receiver features. New sender and receiver variants can occur through mutation, plasticity, hybridization and cultural innovation, and the initial conditions of the sender, the receiver and the environment then dictate whether a novel cue becomes a signal. New features may arise in the sender, the receiver or both simultaneously. We contend that it may be easier than assumed to evolve new sexual signals because sexual signals may be arbitrary, sexual conflict is common and receivers are capable of perceiving much more of the world than just existing sexual signals. Additionally, changes in the signalling environment can approximate both signal and receiver changes through a change in transmission characteristics of a given environment or the use of new environments. The Anthropocene has led to wide-scale disruption of the environment and may thus generate opportunity to directly observe the evolution of new signals to address questions that are beyond the reach of phylogenetic approaches.


Subject(s)
Animal Communication , Biological Evolution , Animals , Communication , Phenotype , Phylogeny
4.
Mol Ecol ; 28(18): 4317-4334, 2019 09.
Article in English | MEDLINE | ID: mdl-31483075

ABSTRACT

Population divergence can occur due to mechanisms associated with geographic isolation and/or due to selection associated with different ecological niches. Much of the evidence for selection-driven speciation has come from studies of specialist insect herbivores that use different host plant species; however, the influence of host plant use on population divergence of generalist herbivores remains poorly understood. We tested how diet breadth, host plant species and geographic distance influence population divergence of the fall webworm (Hyphantria cunea; FW). FW is a broadly distributed, extreme generalist herbivore consisting of two morphotypes that have been argued to represent two different species: black-headed and red-headed. We characterized the differentiation of FW populations at two geographic scales. We first analysed the influence of host plant and geographic distance on genetic divergence across a broad continental scale for both colour types. We further analysed the influence of host plant, diet breadth and geographic distance on divergence at a finer geographic scale focusing on red-headed FW in Colorado. We found clear genetic and morphological distinction between red- and black-headed FW, and Colorado FW formed a genetic cluster distinct from other locations. Although both geographic distance and host plant use were correlated with genetic distance, geographic distance accounted for up to 3× more variation in genetic distance than did host plant use. As a rare study investigating the genetic structure of a widespread generalist herbivore over a broad geographic range (up to 3,000 km), our study supports a strong role for geographic isolation in divergence in this system.


Subject(s)
Genetics, Population , Geography , Herbivory/genetics , Host-Parasite Interactions/genetics , Moths/genetics , Plants/parasitology , Animals , Diet , Moths/anatomy & histology , Phylogeny , United States
5.
Glob Chang Biol ; 25(6): 1957-1966, 2019 06.
Article in English | MEDLINE | ID: mdl-30825350

ABSTRACT

When environments change rapidly, adaptive phenotypic plasticity can ameliorate negative effects of environmental change on survival and reproduction. Recent evidence suggests, however, that plastic responses to human-induced environmental change are often maladaptive or insufficient to overcome novel selection pressures. Anthropogenic noise is a ubiquitous and expanding disturbance with demonstrated effects on fitness-related traits of animals like stress responses, foraging, vigilance, and pairing success. Elucidating the lifetime fitness effects of noise has been challenging because longer-lived vertebrate systems are typically studied in this context. Here, we follow noise-stressed invertebrates throughout their lives, assessing a comprehensive suite of life history traits, and ultimately, lifetime number of surviving offspring. We reared field crickets, Teleogryllus oceanicus, in masking traffic noise, traffic noise from which we removed frequencies that spectrally overlap with the crickets' mate location song and peak hearing (nonmasking), or silence. We found that exposure to masking noise delayed maturity and reduced adult lifespan; crickets exposed to masking noise spent 23% more time in juvenile stages and 13% less time as reproductive adults than those exposed to no traffic noise. Chronic lifetime exposure to noise, however, did not affect lifetime reproductive output (number of eggs or surviving offspring), perhaps because mating provided females a substantial longevity benefit. Nevertheless, these results are concerning as they highlight multiple ways in which traffic noise may reduce invertebrate fitness. We encourage researchers to consider effects of anthropogenic disturbance on growth, survival, and reproductive traits simultaneously because changes in these traits may amplify or nullify one another.


Subject(s)
Gryllidae/physiology , Noise , Animals , Female , Hearing , Humans , Longevity , Male , Reproduction/physiology
6.
Am Nat ; 192(6): 773-782, 2018 12.
Article in English | MEDLINE | ID: mdl-30444653

ABSTRACT

Opportunities to observe contemporary signal change are incredibly rare but critical for understanding how diversity is created and maintained. We discovered a population of the Pacific field cricket (Teleogryllus oceanicus) with a newly evolved song (purring), different from any known cricket. Male crickets use song to attract females from afar and to court females once near. Teleogryllus oceanicus is well known for sexual signal evolution, as exemplified by a recent signal loss. In this study, we characterized the new purring sound and investigated the role of the purr in long-distance and short-distance communication. The purring sound differed from typical ancestral calls in peak frequency, amplitude, and bandwidth. Further, the long-distance purring song facilitated mate location, though the role of courtship purring song is less clear. Our discovery of purring male crickets is an unprecedented opportunity to watch the emergence of a newly evolved sexual signal unfold in real time and has potential to illuminate the mechanisms by which evolutionary novelties arise and coevolve between the sexes.


Subject(s)
Biological Evolution , Gryllidae/physiology , Vocalization, Animal , Animals , Female , Hawaii , Male , Sexual Behavior, Animal , Wings, Animal/anatomy & histology
7.
Proc Biol Sci ; 285(1872)2018 02 14.
Article in English | MEDLINE | ID: mdl-29436498

ABSTRACT

In many cooperatively breeding animals, subordinate group members have lower reproductive capacity than dominant group members. Theory suggests subordinates may downregulate their reproductive capacity because dominants punish subordinates who maintain high fertility. However, there is little direct experimental evidence that dominants cause physiological suppression in subordinates. Here, we experimentally test how social interactions influence subordinate reproductive hormones in Polistes dominula paper wasps. Polistes dominula queens commonly found nests in cooperative groups where the dominant queen is more fertile than the subordinate queen. In this study, we randomly assigned wasps to cooperative groups, assessed dominance behaviour during group formation, then measured levels of juvenile hormone (JH), a hormone that mediates Polistes fertility. Within three hours, lowest ranking subordinates had less JH than dominants or solitary controls, indicating that group formation caused rapid JH reduction in low-ranking subordinates. In a second experiment, we measured the behavioural consequences of experimentally increasing subordinate JH. Subordinates with high JH-titres received significantly more aggression than control subordinates or subordinates from groups where the dominant's JH was increased. These results suggest that dominants aggressively punished subordinates who attempted to maintain high fertility. Low-ranked subordinates may rapidly downregulate reproductive capacity to reduce costly social interactions with dominants. Rapid modulation of subordinate reproductive physiology may be an important adaptation to facilitate the formation of stable, cooperative groups.


Subject(s)
Down-Regulation , Juvenile Hormones/metabolism , Wasps/physiology , Adaptation, Physiological , Animals , Cooperative Behavior , Female , Interpersonal Relations , Reproduction , Social Dominance
8.
Biol Lett ; 14(2)2018 02.
Article in English | MEDLINE | ID: mdl-29491025

ABSTRACT

Phenotypic plasticity facilitates survival and reproduction in rapidly changing and novel environments. Traffic noise spectrally overlaps with (i.e. masks) the sounds used by many acoustically signalling organisms to locate and secure mates. To determine if pre-reproductive exposure to noise improves adult performance in noisy environments, we reared field crickets (Teleogryllus oceanicus) in one of three noise environments: masking traffic noise, traffic noise from which frequencies that spectrally overlap with the crickets' song were removed (non-masking), or silence. At reproductive maturity, we tested female mate location ability under one of the same three acoustic conditions. We found that exposure to noise during rearing hindered female location of mates, regardless of the acoustic environment at testing. Females reared in masking noise took 80% longer than females reared in silence to locate a simulated singing male who was less than 1 m away. Impaired mate location ability can be added to a growing list of fitness costs associated with anthropogenic noise, alongside reductions in pairing success, nesting success and offspring survival.


Subject(s)
Gryllidae/radiation effects , Noise , Sexual Behavior, Animal/radiation effects , Acoustics , Animals , Life Cycle Stages/radiation effects , Vocalization, Animal
9.
BMC Evol Biol ; 15: 200, 2015 Sep 18.
Article in English | MEDLINE | ID: mdl-26385337

ABSTRACT

BACKGROUND: Sexual selection is largely driven by the availability of mates. Theory predicts that male competition and female choice should be density-dependent, with males competing more intensely at relatively high density, and females becoming increasingly discriminating when there are more males from whom to choose. Evidence for flexible mating decisions is growing, but we do not understand how environmental variation is incorporated into mate sampling strategies. We mimicked threespine stickleback (Gasterosteus aculeatus) breeding conditions in pools with high and low densities of nesting males and allowed females to search for mates to determine whether 1) mate search strategies change with the density of breeding males and 2) pre-copulatory components of mate choice (signalling, competition, search patterns, and mating decisions) are modified in parallel. RESULTS: While females sampled more males at high male density, suggesting greater opportunity for sexual selection, the expanded search did not result in females choosing males with more attractive sexual signals. This is likely because red throat colouration was twice as great when half as many males competed. Instead, females chose similarly at high and low male density, using a relative strategy to compare male traits amongst potential suitors. Reduced throat colour could reflect a trade-off with costly male competition. However, we did not observe more intense competition at higher relative density. Density-dependent signalling appears largely responsible for females associating with males who have more attractive signals at low density. If we lacked knowledge of plasticity in signalling, we might have concluded that females are more discriminating at low male density. CONCLUSIONS: To understand interactions between mate choice and population dynamics, we should consider how components of mate choice that precede the mating decision interact.


Subject(s)
Mating Preference, Animal , Smegmamorpha/physiology , Animals , Female , Male , Nesting Behavior , Sexual Behavior, Animal
10.
Evolution ; 78(5): 835-848, 2024 May 01.
Article in English | MEDLINE | ID: mdl-38436989

ABSTRACT

Understanding how the early stages of sexual signal diversification proceed is critically important because these microevolutionary dynamics directly shape species trajectories and impact macroevolutionary patterns. Unfortunately, studying this is challenging because signals involve complex interactions between behavior, morphology, and physiology, much of which can only be measured in real-time. In Hawaii, male Pacific field cricket song attracts both females and a deadly parasitoid fly. Over the past two decades, there has been a marked increase in signal variation in Hawaiian populations of these crickets, including novel male morphs with distinct mating songs. We capitalize on this rare opportunity to track changes in morph composition over time in a population with three novel morphs, investigating how mate and parasitoid attraction (components of sexual and natural selection) may shape signal evolution. We find dramatic fluctuation in morph proportions over the three years of the study, including the arrival and rapid increase of one novel morph. Natural and sexual selection pressures act differently among morphs, with some more attractive to mates and others more protected from parasitism. Collectively, our results suggest that differential protection from parasitism among morphs, rather than mate attraction, aligns with recent patterns of phenotypic change in the wild.


Subject(s)
Gryllidae , Animals , Gryllidae/physiology , Gryllidae/genetics , Male , Female , Selection, Genetic , Sexual Selection , Biological Evolution , Mating Preference, Animal , Hawaii , Vocalization, Animal , Diptera/physiology
11.
BMC Ecol Evol ; 23(1): 78, 2023 12 20.
Article in English | MEDLINE | ID: mdl-38124034

ABSTRACT

BACKGROUND: Anthropogenic habitat change is occurring rapidly, and organisms can respond through within-generation responses that improve the match between their phenotype and the novel conditions they encounter. But, plastic responses can be adaptive or maladaptive and are most likely to be adaptive only when contemporary conditions reasonably mimic something experienced historically to which a response has already evolved. Noise pollution is a ubiquitous anthropogenic stressor that accompanies expanding urbanization. We tested whether the amplitude of traffic noise influences a suite of fitness-related traits (e.g. survival, life history, reproductive investment, immunity) and whether that depends on the life stage at which the noise is experienced (juvenile or adult). Our treatments mimic the conditions experienced by animals living in urban roadside environments with variable vehicle types, but continuous movement of traffic. We used the Pacific field cricket, an acoustically communicating insect that was previously shown to experience some negative behavioral and life history responses to very loud, variable traffic noise, as a model system. RESULTS: After exposing crickets to one of four traffic noise levels (silence, 50dBA, 60dBA, and 70dBA which are commonly experienced in their natural environment) during development, at adulthood, or both, we measured a comprehensive suite of fifteen fitness-related traits. We found that survival to adulthood was lower under some noise treatments than under silence, and that the number of live offspring hatched depended on the interaction between a female's juvenile and adult exposure to traffic noise. Both of these suggest that our noise treatments were indeed a stressor. However, we found no evidence of negative or positive fitness effects of noise on the other thirteen measured traits. CONCLUSIONS: Our results suggest that, in contrast to previous work with loud, variable traffic noise, when noise exposure is relatively constant, plasticity may be sufficient to buffer many negative fitness effects and/or animals may be able to habituate to these conditions, regardless of amplitude. Our work highlights the importance of understanding how the particular characteristics of noise experienced by animals influence their biological responses and provides insight into how commensal animals thrive in human-dominated habitats.


Subject(s)
Noise, Transportation , Animals , Female , Humans , Noise, Transportation/adverse effects , Reproduction/physiology , Environment , Ecosystem , Phenotype
12.
Evol Lett ; 6(6): 474-489, 2022 Dec.
Article in English | MEDLINE | ID: mdl-36579170

ABSTRACT

How novel phenotypes evolve is challenging to imagine because traits are often underlain by numerous integrated phenotypic components, and changes to any one form can disrupt the function of the entire module. Yet novel phenotypes do emerge, and research on adaptive phenotypic evolution suggests that complex traits can diverge while either maintaining existing form-function relationships or through innovations that alter form-function relationships. How these alternate routes contribute to sexual signal evolution is poorly understood, despite the role of sexual signals in generating biodiversity. In Hawaiian populations of the Pacific field cricket, male song attracts both female crickets and a deadly acoustically orienting parasitoid fly. In response to this conflict between natural and sexual selection, male crickets have evolved altered wing morphologies multiple times, resulting in loss and dramatic alteration of sexual signals. More recently, we and others have observed a radical increase in sexual signal variation and the underlying morphological structures that produce song. We conducted the first combined analysis of form (wing morphology), function (emergent signal), and receiver responses to characterize novel variation, test alternative hypotheses about form-function relationships (Form-Function Continuity vs. Form-Function Decoupling), and investigate underlying mechanistic changes and fitness consequences of novel signals. We identified three sound-producing male morphs (one previously undescribed, named "rattling") and found that relationships between morphology and signals have been rewired (Form-Function Decoupling), rapidly and repeatedly, through the gain, loss, and alteration of morphological structures, facilitating the production of signals that exist in novel phenotypic space. By integrating across a hierarchy of phenotypes, we uncovered divergent morphs with unique solutions to the challenge of attracting mates while evading fatal parasitism.

13.
Ecol Evol ; 12(8): e9193, 2022 Aug.
Article in English | MEDLINE | ID: mdl-35979522

ABSTRACT

Animals eavesdrop on signals and cues generated by prey, predators, hosts, parasites, competing species, and conspecifics, and the conspicuousness of sexual signals makes them particularly susceptible. Yet, when sexual signals evolve, most attention is paid to impacts on intended receivers (potential mates) rather than fitness consequences for eavesdroppers. Using the rapidly evolving interaction between the Pacific field cricket, Teleogryllus oceanicus, and the parasitoid fly, Ormia ochracea, we asked how parasitoids initially respond to novel changes in host signals. We recently discovered a novel sexual signal, purring song, in Hawaiian populations of T. oceanicus that appears to have evolved because it protects the cricket from the parasitoid while still allowing males to attract female crickets for mating. In Hawaii, there are no known alternative hosts for the parasitoid, so we would expect flies to be under selection to detect and attend to the new purring song. We used complementary field and laboratory phonotaxis experiments to test fly responses to purring songs that varied in many dimensions, as well as to ancestral song. We found that flies strongly prefer ancestral song over purring songs in both the field and the lab, but we caught more flies to purring songs in the field than reported in previous work, indicating that flies may be exerting some selective pressure on the novel song. When played at realistic amplitudes, we found no preferences-flies responded equally to all purrs that varied in frequency, broadbandedness, and temporal measures. However, our lab experiment did reveal the first evidence of preference for purring song amplitude, as flies were more attracted to purrs played at amplitudes greater than naturally occurring purring songs. As purring becomes more common throughout Hawaii, flies that can use purring song to locate hosts should be favored by selection and increase in frequency.

14.
Nat Commun ; 12(1): 797, 2021 02 04.
Article in English | MEDLINE | ID: mdl-33542210

ABSTRACT

Inadvertent cues can be refined into signals through coevolution between signalers and receivers, yet the earliest steps in this process remain elusive. In Hawaiian populations of the Pacific field cricket, a new morph producing a novel and incredibly variable song (purring) has spread across islands. Here we characterize the current sexual and natural selection landscape acting on the novel signal by (1) determining fitness advantages of purring through attraction to mates and protection from a prominent deadly natural enemy, and (2) testing alternative hypotheses about the strength and form of selection acting on the novel signal. In field studies, female crickets respond positively to purrs, but eavesdropping parasitoid flies do not, suggesting purring may allow private communication among crickets. Contrary to the sensory bias and preference for novelty hypotheses, preference functions (selective pressure) are nearly flat, driven by extreme inter-individual variation in function shape. Our study offers a rare empirical test of the roles of natural and sexual selection in the earliest stages of signal evolution.


Subject(s)
Gryllidae/physiology , Mating Preference, Animal/physiology , Selection, Genetic/physiology , Vocalization, Animal/physiology , Animals , Diptera/physiology , Female , Genetic Fitness , Gryllidae/parasitology , Hawaii , Male , Wings, Animal/physiology
15.
Ecol Evol ; 11(15): 10320-10326, 2021 Aug.
Article in English | MEDLINE | ID: mdl-34367577

ABSTRACT

Anthropogenic disturbances associated with urban ecosystems can create favorable conditions for populations of some invasive plant species. Light pollution is one of these disturbances, but how it affects the growth and establishment of invasive plant populations is unknown. Cheatgrass (Bromus tectorum) is a problematic invasive species where it has displaced native grassland communities in the United States, but to our knowledge, there have been no studies of the ecological factors that affect cheatgrass presence in urban ecosystems. We conducted field surveys in urban alleys in Denver, Colorado, to compare the presence of cheatgrass at sites with and without artificial light at night (hereafter artificial light) from streetlights. These streetlights are mounted on utility poles, which cause ground disturbance when installed in alleys; we were able to test the independent effect of poles on cheatgrass establishment because not all poles have streetlights on them. We found that cheatgrass was positively associated with the presence of streetlights and to a lesser extent poles. In addition to cheatgrass, we also found that other plants were positively associated with the presence of both poles and streetlights. Our results suggest that artificial light may benefit the occurrence of cheatgrass and other plant species in urban settings. While invasive populations of cheatgrass in wild habitats attract the most attention from managers, we suggest more consideration for this grass in urban environments where its growth and establishment benefit from anthropogenic changes.

16.
Naturwissenschaften ; 97(1): 53-61, 2010 Jan.
Article in English | MEDLINE | ID: mdl-19777200

ABSTRACT

The auditory thresholds of the AN2 interneuron and the behavioural thresholds of the anti-bat flight-steering responses that this cell evokes are less sensitive in female Pacific field crickets that live where bats have never existed (Moorea) compared with individuals subjected to intense levels of bat predation (Australia). In contrast, the sensitivity of the auditory interneuron, ON1 which participates in the processing of both social signals and bat calls, and the thresholds for flight orientation to a model of the calling song of male crickets show few differences between the two populations. Genetic analyses confirm that the two populations are significantly distinct, and we conclude that the absence of bats has caused partial regression in the nervous control of a defensive behaviour in this insect. This study represents the first examination of natural evolutionary regression in the neural basis of a behaviour along a selection gradient within a single species.


Subject(s)
Chiroptera/physiology , Gryllidae/physiology , Hearing/physiology , Animals , Auditory Threshold , Australia , Behavior, Animal , DNA/genetics , DNA Primers , Ecosystem , Feedback, Sensory/physiology , Female , Flight, Animal/physiology , Genetic Carrier Screening , Gryllidae/genetics , Linkage Disequilibrium , Male , Muscle, Skeletal/physiology , Pacific Islands , Population Density
17.
Evolution ; 74(2): 404-418, 2020 02.
Article in English | MEDLINE | ID: mdl-31883271

ABSTRACT

Parental experience alters survival-related phenotypes of offspring in both adaptive and nonadaptive ways, yielding rapid inter- and transgenerational fitness effects. Yet, fitness comprises survival and reproduction, and parental effects on mating decisions could alter the strength and direction of sexual selection, affecting long-term evolutionary trajectories. We used a full factorial design in which threespine stickleback (Gasterosteus aculeatus) mothers, fathers, both, or neither were exposed to a model predator at developmentally appropriate times to test for predator-induced maternal, paternal, and joint parental effects on daughters' mating behavior. We tested the responsiveness, preferences, and mate choices of adult daughters in no-choice trials with wild-caught males who had varied sexual signals. Maternal and paternal predator exposure independently yielded daughters who preferred males who were intermediate in conspicuousness (with duller nuptial coloration and who courted less vigorously), relaxing the typical preference for the most conspicuous males. The combined effects of maternal and paternal predator exposure were not cumulative; when both parents were predator exposed, single-parent effects on mate preferences were reversed. Thus, we cannot assume that maternal and paternal effects additively combine to produce "parental" effects. Further, joint parental predator exposure yielded daughters who were three times less likely to mate at all. Stress-induced intergenerational parental effects on reproductive decisions such as those observed here may potentiate rapid transgenerational responses to novel and changing mating environments.


Subject(s)
Maternal Inheritance , Mating Preference, Animal , Paternal Inheritance , Smegmamorpha/physiology , Animals , Female , Food Chain , Male , Phenotype , Smegmamorpha/genetics
18.
Philos Trans R Soc Lond B Biol Sci ; 375(1806): 20190546, 2020 08 31.
Article in English | MEDLINE | ID: mdl-32654644

ABSTRACT

Preference divergence is thought to contribute to reproductive isolation. Ecology can alter the way selection acts on female preferences, making them most likely to diverge when ecological conditions vary among populations. We present a novel mechanism for ecologically dependent sexual selection, termed 'the ecological stage' to highlight its ecological dependence. Our hypothesized mechanism emphasizes that males and females interact over mating in a specific ecological context, and different ecological conditions change the costs and benefits of mating interactions, selecting for different preferences in distinct environments and different male traits, especially when traits are condition dependent. We test key predictions of this mechanism in a sympatric three-spine stickleback species pair. We used a maternal half-sib split-clutch design for both species, mating females to attractive and unattractive males and raising progeny on alternate diets that mimic the specialized diets of the species in nature. We estimated the benefits of mate choice for an indicator trait (male nuptial colour) by measuring many fitness components across the lifetimes of both sons and daughters from these crosses. We analysed fitness data using a combination of aster and mixed models. We found that many benefits of mating with high-colour males depended on both species and diet. These results support the ecological stage hypothesis for sticklebacks. Finally, we discuss the potential role of this mechanism for other taxa and highlight its ability to enhance reproductive isolation as speciation proceeds, thus facilitating the evolution of strong reproductive isolation. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.


Subject(s)
Genetic Speciation , Mating Preference, Animal , Reproductive Isolation , Smegmamorpha/genetics , Sympatry/genetics , Animals , Female , Male
19.
Ecol Evol ; 10(6): 2900-2916, 2020 Mar.
Article in English | MEDLINE | ID: mdl-32211164

ABSTRACT

By studying systems in their earliest stages of differentiation, we can learn about the evolutionary forces acting within and among populations and how those forces could contribute to reproductive isolation. Such an understanding would help us to better discern and predict how selection leads to the maintenance of multiple morphs within a species, rather than speciation. The postglacial adaptive radiation of the threespine stickleback (Gasterosteus aculeatus) is one of the best-studied cases of evolutionary diversification and rapid, repeated speciation. Following deglaciation, marine stickleback have continually invaded freshwater habitats across the northern hemisphere and established resident populations that diverged innumerable times from their oceanic ancestors. Independent freshwater colonization events have yielded broadly parallel patterns of morphological differences in freshwater and marine stickleback. However, there is also much phenotypic diversity within and among freshwater populations. We studied a lesser-known freshwater "species pair" found in southwest Washington, where male stickleback in numerous locations have lost the ancestral red sexual signal and instead develop black nuptial coloration. We measured phenotypic variation in a suite of traits across sites where red and black stickleback do not overlap in distribution and at one site where they historically co-occurred. We found substantial phenotypic divergence between red and black morphs in noncolor traits including shape and lateral plating, and additionally find evidence that supports the hypothesis of sensory drive as the mechanism responsible for the evolutionary switch in color from red to black. A newly described third "mixed" morph in Connor Creek, Washington, differs in head shape and size from the red and black morphs, and we suggest that their characteristics are most consistent with hybridization between anadromous and freshwater stickleback. These results lay the foundation for future investigation of the underlying genetic basis of this phenotypic divergence as well as the evolutionary processes that may drive, maintain, or limit divergence among morphs.

20.
Curr Zool ; 65(3): 285-293, 2019 Jun.
Article in English | MEDLINE | ID: mdl-31263487

ABSTRACT

Male cognition has gained recognition as an important potential player in sexual selection. A number of studies have found positive correlations between male sexual signals and cognitive performance and/or female preferences for males with better cognitive performance, although other studies have not found these relationships. Sex roles can differ dramatically, and sex differences in selection on cognition likely follow from the different tasks associated with these sex roles. Here, using threespine stickleback Gasterosteus aculeatus, a species with clearly divergent sex roles and mutual mate choice, we focus on the cognitive trait inhibitory control because males must differentially respond to reproductive females versus other sticklebacks while defending territories and refrain from eating eggs and fry while performing paternal care. We presented fish with a detour task four times over a period of 7 days, allowing us to assess initial inhibitory control and improvement over time. We ask 1) whether there are sex differences in inhibitory control and 2) whether male mate choice is associated with female inhibitory control. Although males outperformed females on three different measures of detour task performance across four trials, these differences were largely explained by males being less neophobic than females. Females took more trials to successfully solve the detour task, even after accounting for sex differences in neophobia. Female cognitive abilities, however, were unrelated to the vigor with which males courted them. The equivocal results regarding sex differences in cognitive ability suggest further study given the very different selection pressures each sex experiences.

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