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1.
Ecol Lett ; 27(1): e14341, 2024 Jan.
Article in English | MEDLINE | ID: mdl-37988323

ABSTRACT

Males are often predicted to prefer virgin over non-virgin females because of the reduced risk of sperm competition. Does this prediction hold across studies? Our systematic meta-analysis of 138 studies, mainly conducted in invertebrates, confirms that males generally prefer virgin females. However, males preferred virgin females even in species with last male sperm precedence, suggesting that sperm competition alone does not drive male preferences. Furthermore, our results suggest that males may reject mated females even when no alternative exists. Preference for virgins is unlikely to influence female reproductive success since virginity cannot be selected for, but strong preference for virgin females could swamp or reinforce selection on other traits. Our results add to growing evidence that males are not indiscriminate in mating. However, given the unexplained heterogeneity in effect sizes, we urge caution in assuming that males will prefer virgins and recommend considering the natural context of mating decisions.


Subject(s)
Semen , Sexual Behavior, Animal , Animals , Male , Female , Reproduction , Spermatozoa , Phenotype
2.
Behav Ecol ; 35(1): arad098, 2024.
Article in English | MEDLINE | ID: mdl-38144906

ABSTRACT

Circadian rhythms are ubiquitous in nature and endogenous circadian clocks drive the daily expression of many fitness-related behaviors. However, little is known about whether such traits are targets of selection imposed by natural enemies. In Hawaiian populations of the nocturnally active Pacific field cricket (Teleogryllus oceanicus), males sing to attract mates, yet sexually selected singing rhythms are also subject to natural selection from the acoustically orienting and deadly parasitoid fly, Ormia ochracea. Here, we use T. oceanicus to test whether singing rhythms are endogenous and scheduled by circadian clocks, making them possible targets of selection imposed by flies. We also develop a novel audio-to-circadian analysis pipeline, capable of extracting useful parameters from which to train machine learning algorithms and process large quantities of audio data. Singing rhythms fulfilled all criteria for endogenous circadian clock control, including being driven by photoschedule, self-sustained periodicity of approximately 24 h, and being robust to variation in temperature. Furthermore, singing rhythms varied across individuals, which might suggest genetic variation on which natural and sexual selection pressures can act. Sexual signals and ornaments are well-known targets of selection by natural enemies, but our findings indicate that the circadian timing of those traits' expression may also determine fitness.

3.
Proc Biol Sci ; 290(1997): 20230002, 2023 04 26.
Article in English | MEDLINE | ID: mdl-37122255

ABSTRACT

Same-sex sexual behaviour (SSB) occurs in many animals and is often treated as an anomaly requiring special explanation. One common explanation for SSB is mistaken identity. However, animals make similar 'mistakes' in other contexts-such as attempting to mate with immature individuals or inanimate objects. Framing such behaviours as 'mistakes' risks misinterpreting how animals make flexible mating decisions. Here we make a case for an alternative approach to thinking about SSB by instead considering an individual's mating filter. A broad filter means directing courtship toward anything that resembles a potential mate, whilst a narrow filter means only courting with receptive targets. We illustrate this approach by examining the mating filters of male Pacific field crickets (Teleogryllus oceanicus). We find that males engage in SSB but also misdirect courtship toward juveniles (but not plastic crickets). This finding suggests that SSB is not an anomaly and is better considered alongside other misdirected behaviours. We argue that by viewing misdirected behaviours through the lens of mating filters rather than as 'mistakes' we can build a more nuanced understanding of reproductive behaviour and begin to determine when having a broader mating filter can be advantageous.


Subject(s)
Gryllidae , Animals , Male , Reproduction , Courtship , Sexual Behavior, Animal
4.
Biol Rev Camb Philos Soc ; 97(3): 1161-1178, 2022 06.
Article in English | MEDLINE | ID: mdl-35094460

ABSTRACT

Animal migration (round-trip, predictable movements) takes individuals across space and time, bringing them into contact with new communities of organisms. In particular, migratory movements shape (and are shaped by) the costs and risk of parasite transmission. Unfortunately, our understanding of how migration and parasite infection interact has not proceeded evenly. Although numerous conceptual frameworks (e.g. mathematical models) have been developed, most empirical evidence of migration-parasite interactions are drawn from pre-existing empirical studies that were conducted using other conceptual frameworks, which limits our understanding. Here, we synthesise and analyse existing work, and then provide a roadmap for future (especially empirical) studies. First, we synthesise the conceptual frameworks that have been developed to understand interactions between migration and parasites (e.g. migratory exposure, escape, allopatry, recovery, culling, separation, stalling and relapse). Second, we highlight current challenges to studying migration and parasites empirically, and to integrating empirical and theoretical perspectives, particularly emphasizing the challenge of feedback loops. Finally, we provide a guide to overcoming these challenges in empirical studies, using comparative, observational and experimental approaches. Beyond guiding future empirical work, this review aims to inspire stronger collaboration between empiricists and theorists studying the intersection of migration and parasite infection. Such collaboration will help overcome current limits to our understanding of how migration and parasites interact, and allow us to predict how these critical ecological processes will change in the future.


Subject(s)
Parasites , Parasitic Diseases , Animal Migration , Animals , Host-Parasite Interactions , Models, Theoretical
5.
J Evol Biol ; 34(3): 549-557, 2021 03.
Article in English | MEDLINE | ID: mdl-33484624

ABSTRACT

Associations between heritable polymorphisms and life-history traits, such as development time or reproductive investment, may play an underappreciated role in maintaining polymorphic systems. This is because selection acting on a particular morph could be bolstered or disrupted by correlated changes in life history or vice versa. In a Hawaiian population of the Pacific field cricket (Teleogryllus oceanicus), a novel mutation (flatwing) on the X-chromosome is responsible for a heritable polymorphism in male wing structure. We used laboratory cricket colonies fixed for male wing morph to investigate whether males and females bearing the flatwing or normal-wing (wild-type) allele differed in their life-history traits. We found that flatwing males developed faster and had heavier testes than normal-wings, whereas flatwing homozygous females developed slower and had lighter reproductive tissues than normal-wing homozygous females. Our results advance our understanding of the evolution of polymorphisms by demonstrating that the genetic change responsible for a reproductive polymorphism can also have consequences for fundamental life-history traits in both males and females.


Subject(s)
Genitalia/growth & development , Gryllidae/genetics , Life History Traits , Wings, Animal/growth & development , Animals , Female , Gryllidae/growth & development , Male , Polymorphism, Genetic , Reproduction
6.
Ecol Evol ; 11(24): 17625-17650, 2021 Dec.
Article in English | MEDLINE | ID: mdl-35003629

ABSTRACT

Urbanization is rapidly altering landscapes worldwide, changing environmental conditions, and creating novel selection pressures for many organisms. Local environmental conditions affect the expression and evolution of sexual signals and mating behaviors; changes in such traits have important evolutionary consequences because of their effect on reproduction. In this review, we synthesize research investigating how sexual communication is affected by the environmental changes associated with urbanization-including pollution from noise, light, and heavy metals, habitat fragmentation, impervious surfaces, urban heat islands, and changes in resources and predation. Urbanization often has negative effects on sexual communication through signal masking, altering condition-dependent signal expression, and weakening female preferences. Though there are documented instances of seemingly adaptive shifts in trait expression, the ultimate impact on fitness is rarely tested. The field of urban evolution is still relatively young, and most work has tested whether differences occur in response to various aspects of urbanization. There is limited information available about whether these responses represent phenotypic plasticity or genetic changes, and the extent to which observed shifts in sexual communication affect reproductive fitness. Our understanding of how sexual selection operates in novel, urbanized environments would be bolstered by more studies that perform common garden studies and reciprocal transplants, and that simultaneously evaluate multiple environmental factors to tease out causal drivers of observed phenotypic shifts. Urbanization provides a unique testing ground for evolutionary biologists to study the interplay between ecology and sexual selection, and we suggest that more researchers take advantage of these natural experiments. Furthermore, understanding how sexual communication and mating systems differ between cities and rural areas can offer insights on how to mitigate negative, and accentuate positive, consequences of urban expansion on the biota, and provide new opportunities to underscore the relevance of evolutionary biology in the Anthropocene.

7.
Ecology ; 102(2): e03229, 2021 02.
Article in English | MEDLINE | ID: mdl-33098657

ABSTRACT

Migration can allow individuals to escape parasite infection, which can lead to a lower infection probability (prevalence) in a population and/or fewer parasites per individual (intensity). Because individuals with more parasites often have lower survival and/or fecundity, infection intensity shapes the life-history trade-offs determining when migration is favored as a strategy to escape infection. Yet, most theory relies on susceptible-infected (SI) modeling frameworks, defining individuals as either healthy or infected, ignoring details of infection intensity. Here, we develop a novel modeling approach that captures infection intensity as a spectrum, and ask under what conditions migration evolves as function of how infection intensity changes over time. We show that relative timescales of migration and infection accumulation determine when migration is favored. We also find that population-level heterogeneity in infection intensity can lead to partial migration, where less-infected individuals migrate while more infected individuals remain resident. Our model is one of the first to consider how infection intensity can lead to migration. Our results frame migratory escape in light of infection intensity rather than prevalence, thus demonstrating that decreased infection intensity should be considered a benefit of migration, alongside other typical drivers of migration.


Subject(s)
Parasites , Animal Migration , Animals , Humans
8.
Ecol Evol ; 10(23): 13312-13326, 2020 Dec.
Article in English | MEDLINE | ID: mdl-33304539

ABSTRACT

Among the parasites of insects, endoparasitoids impose a costly challenge to host defenses because they use their host's body for the development and maturation of their eggs or larvae, and ultimately kill the host. Tachinid flies are highly specialized acoustically orienting parasitoids, with first instar mobile larvae that burrow into the host's body to feed. We investigated the possibility that Teleogryllus oceanicus field crickets employ postinfestation strategies to maximize survival when infested with the larvae of the parasitoid fly Ormia ochracea. Using crickets from the Hawaiian Islands of Kauai, where the parasitoid is present, and crickets from the Cook Islands (Mangaia), where the parasitoid is absent, we evaluated fitness consequences of infestation by comparing feeding behavior, reproductive capacity, and survival of males experimentally infested with O. ochracea larvae. We also evaluated mechanisms underlying host responses by comparing gene expression in crickets infested with fly larvae for different lengths of time with that of uninfested control crickets. We observed weak population differences in fitness (spermatophore production) and survival (total survival time postinfestation). These responses generally did not show an interaction between population and the number of larva hosts carried or by host body condition. Gene expression patterns also revealed population differences in response to infestation, but we did not find evidence for consistent differences in genes associated with immunity or stress response. One possibility is that any postinfestation evolved resistance does not involve genes associated with these particular functional categories. More likely, these results suggest that coevolution with the fly does not strongly select for either postinfestation resistance or tolerance of parasitoid larvae in male crickets.

10.
Evolution ; 74(5): 1002-1009, 2020 05.
Article in English | MEDLINE | ID: mdl-32187385

ABSTRACT

Pleiotropy between male signals and female preferences can facilitate evolution of sexual communication by maintaining coordination between the sexes. Alternatively, it can favor variation in the mating system, such as a reproductive polymorphism. It is unknown how common either of these scenarios is in nature. In Pacific field crickets (Teleogryllus oceanicus) on Kauai, Hawaii, a mutation (flatwing) that segregates as a single locus is responsible for the rapid loss of song production in males. We used outbred cricket colonies fixed for male wing morph to investigate whether homozygous flatwing and normal-wing (wild-type) females differ in responsiveness to male calling song and propensity to mate when paired with either a flatwing or normal-wing male in the presence or absence of courtship song. Flatwing females were less likely to mount a male than normal-wing females. Females of both genotypes showed a preference for normal-wing males and were more likely to mate in the presence of courtship song; normal-wing females were particularly likely to mate with song. Our results show that negative pleiotropy between obligate male silence and female mating behavior can constrain the evolution of sexual signal loss and contribute to the maintenance of a male reproductive polymorphism in the wild.


Subject(s)
Animal Communication , Genetic Pleiotropy , Gryllidae/physiology , Sexual Behavior, Animal , Animals , Female , Gryllidae/genetics , Male
12.
Ecol Evol ; 9(19): 11476-11493, 2019 Oct.
Article in English | MEDLINE | ID: mdl-31641487

ABSTRACT

Successful geographic range expansion by parasites and parasitoids may also require host range expansion. Thus, the evolutionary advantages of host specialization may trade off against the ability to exploit new host species encountered in new geographic regions. Here, we use molecular techniques and confirmed host records to examine biogeography, population divergence, and host flexibility of the parasitoid fly, Ormia ochracea (Bigot). Gravid females of this fly find their cricket hosts acoustically by eavesdropping on male cricket calling songs; these songs vary greatly among the known host species of crickets. Using both nuclear and mitochondrial genetic markers, we (a) describe the geographical distribution and subdivision of genetic variation in O. ochracea from across the continental United States, the Mexican states of Sonora and Oaxaca, and populations introduced to Hawaii; (b) demonstrate that the distribution of genetic variation among fly populations is consistent with a single widespread species with regional host specialization, rather than locally differentiated cryptic species; (c) identify the more-probable source populations for the flies introduced to the Hawaiian islands; (d) examine genetic variation and substructure within Hawaii; (e) show that among-population geographic, genetic, and host song distances are all correlated; and (f) discuss specialization and lability in host-finding behavior in light of the diversity of cricket songs serving as host cues in different geographically separate populations.

13.
J Evol Biol ; 32(12): 1382-1390, 2019 12.
Article in English | MEDLINE | ID: mdl-31495021

ABSTRACT

Sexual signal evolution may present fitness consequences for the non-signaling sex due to shared genes and altered social conditions, but this is rarely studied in natural populations. On the Hawaiian Island of Kauai, most male Teleogryllus oceanicus (Pacific field crickets) lack the ability to sing because of a novel wing mutation (flatwing) that arose and spread in <20 generations. Obligately silent flatwing males have been highly successful because they avoid detection by a deadly, acoustically-orienting parasitoid fly. Little is known about how the flatwing mutation and resulting song-less acoustic environment affects female fitness. We found that Kauai females carrying the flatwing allele invested less in reproductive tissues and experienced more instances of mating failure than normal-wing-carrying females, though total offspring production did not differ between female genotypes. Females from Oahu (HI, where the parasitoid and flatwing also occur) and Mangaia (an island in the Cook Islands which harbors neither the parasitoid nor flatwing) invested less in reproductive tissues when reared in a song-less acoustic environment. Kauai females did not exhibit this plasticity, perhaps because they have experienced nearly song-less conditions for the past ~15 years following the establishment of flatwing. We show that female T. oceanicus experience a mix of costly and beneficial effects of sexual signal loss, which should help maintain the wing polymorphism in the wild. Our results demonstrate that the non-signaling sex can experience a nuanced set of phenotypic consequences resulting from signal evolution, which can further shape dynamics of sexual signal evolution.


Subject(s)
Gryllidae/physiology , Sexual Behavior, Animal/physiology , Vocalization, Animal/physiology , Animals , Female , Male , Wings, Animal/anatomy & histology
14.
Biol Lett ; 15(7): 20190198, 2019 07 26.
Article in English | MEDLINE | ID: mdl-31362608

ABSTRACT

How sexual traits are gained and lost in the wild remains an important question in evolutionary biology. Pacific field crickets (Teleogryllus oceanicus) in Hawaii provide an unprecedented opportunity to investigate the factors facilitating evolutionary loss of a sexual signal in real time. Natural selection from an acoustically orienting parasitoid fly drove rapid evolution of a novel, silent male morph. While silent (flatwing) males enjoy protection from the fly, they face difficulty attracting mates. We tested how offspring production varies in association with three male attributes affected by the spread of flatwing: wing morph (flatwing or normal-wing), age (flatwings should survive longer than singers) and exposure to calling song during rearing (wild populations with many flatwings lack ambient calling song). Per mating event, flatwings sired more offspring than singers and older males were mounted more quickly by females when presented with standard courtship song. Despite prior work showing that male age and acoustic experience influence sperm characteristics associated with fertilization, age and song exposure had no influence on male offspring production per mating. This represents the first evidence that the silent male morph possesses a reproductive advantage that may help compensate for precopulatory barriers to mate attraction.


Subject(s)
Gryllidae , Vocalization, Animal , Animals , Biological Evolution , Female , Hawaii , Male , Sexual Behavior, Animal , Wings, Animal
15.
Proc Natl Acad Sci U S A ; 116(29): 14413, 2019 07 16.
Article in English | MEDLINE | ID: mdl-31249145

Subject(s)
Plague , Humans , USSR
16.
J Anim Ecol ; 88(10): 1601-1612, 2019 10.
Article in English | MEDLINE | ID: mdl-31220346

ABSTRACT

Most studies on the evolution of migration focus on food, mates and/or climate as factors influencing these movements, whereas negative species interactions such as predators, parasites and pathogens are often ignored. Although infection and its associated costs clearly have the potential to influence migration, thoroughly studying these interactions is challenging without a solid theoretical framework from which to develop testable predictions in natural systems. Here, we aim to understand when parasites favour the evolution of migration. We develop a general model which enables us to explore a broad range of biological conditions and to capture population and infection dynamics over both ecological and evolutionary time-scales. We show that when migration evolves depends on whether the costs of migration and infection are paid in reduced fecundity or survival. Also important are the parasite transmission mode and spatiotemporal dynamics of infection and recovery (if it occurs). Finally, we find that partial migration (where only a fraction of the population migrates) can evolve but only when parasite transmission is density-dependent. Our results highlight the critical, if overlooked, role of parasites in shaping long-distance movement patterns, and suggest that infection should be considered alongside more traditional drivers of migration in both empirical and theoretical studies.


Subject(s)
Infections , Parasites , Animals , Ecology , Host-Parasite Interactions , Models, Theoretical
17.
Evolution ; 73(7): 1482-1489, 2019 07.
Article in English | MEDLINE | ID: mdl-31243769

ABSTRACT

Evolutionary biologists commonly seek explanations for how selection drives the emergence of novel traits. Although trait loss is also predicted to occur frequently, few contemporary examples exist. In Hawaii, the Pacific field cricket (Teleogryllus oceanicus) is undergoing adaptive sexual signal loss due to natural selection imposed by eavesdropping parasitoids. Mutant male crickets ("flatwings") cannot sing. We measured the intensity of sexual selection on wing phenotype in a wild population. First, we surveyed the relative abundance of flatwings and "normal-wings" (nonmutants) on Oahu. Then, we bred wild-mated females' offspring to determine both female genotype with respect to the flatwing mutation and the proportion of flatwing males that sired their offspring. We found evidence of strong sexual selection favoring the production of song: females were predominantly homozygous normal-wing, their offspring were sired disproportionately by singing males, and at the population level, flatwing males became less common following a single sexual selection event. We report a selection coefficient describing the total (pre- and postcopulatory) sexual selection favoring normal-wing males in nature. Given the maintenance of the flatwing phenotype in Hawaii in recent years, this substantial sexual selection additionally suggests an approximate strength of opposing natural selection that favors silent males.


Subject(s)
Animal Communication , Gryllidae/physiology , Sexual Behavior, Animal , Animals , Female , Male , Phenotype , Wings, Animal
18.
Proc Biol Sci ; 286(1902): 20190677, 2019 05 15.
Article in English | MEDLINE | ID: mdl-31064302

ABSTRACT

While the reproductive benefits of sexual displays have been widely studied, we have relatively limited evidence of the fitness costs associated with most display traits. Insect cuticular hydrocarbon (CHC) profiles are sexually selected traits that also protect against desiccation. These two functions are thought to oppose each other, with investment in particular compounds believed to increase attractiveness at the expense of compounds that protect against water loss. We investigated this potential trade-off in a quantitative genetic framework using the Australian field cricket, Teleogryllus oceanicus. Several compounds were significantly genetically correlated with either attractiveness or desiccation resistance. Of these compounds, one was negatively genetically correlated with attractiveness but positively genetically correlated with desiccation resistance. Furthermore, scoring each individual's overall CHC profile for its level of attractiveness and desiccation resistance indicated a negative genetic correlation between these multivariate phenotypes. Together, our results provide evidence for a genetic trade-off between sexually and naturally selected functions of the CHC profile. We suggest that the production of an attractive CHC profile may be costly for males, but highlight the need for further work to support this finding experimentally. Genetic covariation between the CHC profile and attractiveness suggests that females can gain attractive sons through female choice.


Subject(s)
Gryllidae/genetics , Hydrocarbons/analysis , Mating Preference, Animal , Selection, Genetic , Animals , Female , Male
19.
Proc Natl Acad Sci U S A ; 116(19): 9155-9163, 2019 05 07.
Article in English | MEDLINE | ID: mdl-31061115

ABSTRACT

Zoonoses, such as plague, are primarily animal diseases that spill over into human populations. While the goal of eradicating such diseases is enticing, historical experience validates abandoning eradication in favor of ecologically based control strategies (which reduce morbidity and mortality to a locally accepted risk level). During the 20th century, one of the most extensive plague-eradication efforts in recorded history was undertaken to enable large-scale changes in land use in the former Soviet Union (including vast areas of central Asia). Despite expending tremendous resources in its attempt to eradicate plague, the Soviet antiplague response gradually abandoned the goal of eradication in favor of plague control linked with developing basic knowledge of plague ecology. Drawing from this experience, we combine new gray-literature sources, historical and recent research, and fieldwork to outline best practices for the control of spillover from zoonoses while minimally disrupting wildlife ecosystems, and we briefly compare the Soviet case with that of endemic plague in the western United States. We argue for the allocation of sufficient resources to maintain ongoing local surveillance, education, and targeted control measures; to incorporate novel technologies selectively; and to use ecological research to inform developing landscape-based models for transmission interruption. We conclude that living with emergent and reemergent zoonotic diseases-switching to control-opens wider possibilities for interrupting spillover while preserving natural ecosystems, encouraging adaptation to local conditions, and using technological tools judiciously and in a cost-effective way.


Subject(s)
Plague/epidemiology , Plague/prevention & control , Animals , Disease Outbreaks , Ecosystem , Humans , Plague/microbiology , Rodentia/microbiology , Siphonaptera/microbiology , Siphonaptera/physiology , USSR/epidemiology , Yersinia pestis , Zoonoses/epidemiology , Zoonoses/microbiology , Zoonoses/transmission
20.
Nat Ecol Evol ; 3(4): 552-560, 2019 04.
Article in English | MEDLINE | ID: mdl-30886375

ABSTRACT

Biological rhythms coordinate organisms' activities with daily rhythms in the environment. For parasites, this includes rhythms in both the external abiotic environment and the within-host biotic environment. Hosts exhibit rhythms in behaviours and physiologies, including immune responses, and parasites exhibit rhythms in traits underpinning virulence and transmission. Yet, the evolutionary and ecological drivers of rhythms in traits underpinning host defence and parasite offence are largely unknown. Here, we explore how hosts use rhythms to defend against infection, why parasites have rhythms and whether parasites can manipulate host clocks to their own ends. Harnessing host rhythms or disrupting parasite rhythms could be exploited for clinical benefit; we propose an interdisciplinary effort to drive this emerging field forward.


Subject(s)
Biological Evolution , Circadian Rhythm , Host-Parasite Interactions , Animals , Ecology , Humans
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