Reproductive Tactics Research Articles

Morphological Polymorphism Associated with Alternative Reproductive Tactics in a Plethodontid Salamander.

Understanding polymorphism is a central problem in evolution and ecology, and alternative reproductive tactics (ARTs) provide compelling examples for studying the origin and maintenance of behavioral and morphological variation. Much attention has been given to examples where "parasitic" individuals exploit the reproductive investment of "bourgeois" individuals, but some ARTs are instead maintained by environmental heterogeneity, with alternative tactics exhibiting differential fitness in discontinuous reproductive niches. We use genomic, behavioral, karyological, and field observational data to demonstrate one such example in plethodontid salamanders. These ARTs ("searching" and "guarding" males) are associated with different reproductive niches and, unlike most other examples in amphibians, demonstrate substantial morphological differences and inflexibility within a reproductive season. Evidence suggests the existence of these ARTs within three putative species in the two-lined salamander (Eurycea bislineata) species complex, with other members of this clade fixed for one of the two tactics. We highlight directions for future research in this system, including the relationship between these ARTs and parental care.

Mosaic environments shape the distribution of Neotropical freshwater ichthyoplankton

AbstractDam presence results in heterogeneous aquatic environments that probably favour segregation of ichthyoplankton developmental stages. Therefore, the present study tested the hypothesis that dams in the Upper Uruguay River create heterogeneous aquatic environments favouring segregation of ichthyoplankton developmental stages and also separate species with different reproductive tactics. Ichthyoplankton were captured bimonthly during 2002–2015 in 25 sampling stations grouped by fluviometric characteristics. Sampling was performed at night, with cylindrical–conical plankton nets and light traps. After quantifying ichthyoplankton, we identified larvae to the lowest possible taxonomic level and classified them based on developmental stage and reproductive tactics. Egg abundance was higher in lotic environments, preflexion individuals were more abundant in transitional lotic/lentic environments, and the flexion stage was predominant in lentic environments. Larval assemblages consisted mainly of sedentary species or those with short reproductive migrations. Species with similar reproductive tactics occurred in different environments. In conclusion, we provided evidence demonstrating that mosaic environments in the Upper Uruguay River are important for life cycle completion of different fish species. These distinct habitat zones allow for successful spawning and offspring development, thus guaranteeing recruitment.

Social parasitism as an alternative reproductive tactic in a cooperatively breeding cuckoo.

Cooperatively nesting birds are vulnerable to social parasites that lay their eggs in host nests but provide no parental care1-4. Most previous research has focused on the co-evolutionary arms race between host defences and the parasites that attempt to circumvent them5-9, but it remains unclear why females sometimes cooperate and sometimes parasitize, and how parasitic tactics arise in cooperative systems10-12. Here we show that cooperative and parasitic reproductive strategies result in approximately equal fitness pay-offs in the greater ani (Crotophaga major), a long-lived tropical cuckoo, using an 11-year dataset and comprehensive genetic data that enable comparisons of the life-histories of individual females. We found that most females in the population nested cooperatively at the beginning of the breeding season; however, of those birds that had their first nests destroyed, a minority subsequently acted as reproductive parasites. The tendency to parasitize was highly repeatable, which indicates individual specialization. Across years, the fitness pay-offs of the two strategies were approximately equal: females who never parasitized (a 'pure cooperative' strategy) laid larger clutches and fledged more young from their own nests than did birds that both nested and parasitized (a 'mixed' strategy). Our results suggest that the success of parasites is constrained by reproductive trade-offs as well as by host defences, and illustrate how cooperative and parasitic tactics can coexist stably in the same population.

Sperm maturation and male tactic-specific differences in ejaculates in the plainfin midshipman fish Porichthys notatus.

Using the plainfin midshipman fish Porichthys notatus, a species with alternative reproductive tactics (ARTs), we investigated how sperm maturation shapes sperm competitive abilities. We compared sperm performance and morphology before and after final sperm maturation by sampling sperm from the testes and stripped ejaculates of guarders and sneakers. In accordance with sperm competition risk theory, ejaculates from sneaker males had three times as much sperm as ejaculates from guarder males and sneaker males produced faster swimming sperm than guarder males, but this was only the case after final sperm maturation had occurred. Additionally, fully mature sperm found in ejaculates had larger heads and midpieces than sperm found in the testes. These results emphasize the important role played by non-sperm components of an ejaculate in mediating sperm performance and potentially also morphology.

The role of genetic diversity in the evolution and maintenance of environmentally-cued, male alternative reproductive tactics

BackgroundAlternative reproductive tactics (ARTs) are taxonomically pervasive strategies adopted by individuals to maximize reproductive success within populations. Even for conditionally-dependent traits, consensus postulates most ARTs involve both genetic and environmental interactions (GEIs), but to date, quantifying genetic variation underlying the threshold disposing an individual to switch phenotypes in response to an environmental cue has been a difficult undertaking. Our study aims to investigate the origins and maintenance of ARTs within environmentally disparate populations of the microscopic bulb mite, Rhizoglyphus robini, that express ‘fighter’ and ‘scrambler’ male morphs mediated by a complex combination of environmental and genetic factors.ResultsUsing never-before-published individual genetic profiling, we found all individuals across populations are highly inbred with the exception of scrambler males in stressed environments. In fact within the poor environment, scrambler males and females showed no significant difference in genetic differentiation (Fst) compared to all other comparisons, and although fighters were highly divergent from the rest of the population in both poor or rich environments (e.g., Fst, STRUCTURE), fighters demonstrated approximately three times less genetic divergence from the population in poor environments. AMOVA analyses further corroborated significant genetic differentiation across subpopulations, between morphs and sexes, and among subpopulations within each environment.ConclusionOur study provides new insights into the origin of ARTs in the bulb mite, highlighting the importance of GEIs: genetic correlations, epistatic interactions, and sex-specific inbreeding depression across environmental stressors. Asymmetric reproductive output, coupled with the purging of highly inbred individuals during environmental oscillations, also facilitates genetic variation within populations, despite evidence for strong directional selection. This cryptic genetic variation also conceivably facilitates stable population persistence even in the face of spatially or temporally unstable environmental challenges. Ultimately, understanding the genetic context that maintains thresholds, even for conditionally-dependent ARTs, will enhance our understanding of within population variation and our ability to predict responses to selection.

Differential investment in male accessory glands: lessons from a marine fish with alternative reproductive tactics

Male reproductive accessory glands play a number of important roles, including enhancing fertilization success in competitive contexts. Theory predicts that males experiencing greater sperm competition risk (i.e. those adopting the opportunistic tactic) should invest more in accessory glands and ejaculate. However, empirical data show the opposite pattern; males experiencing lower sperm competition risk (i.e. those adopting the conventional guarder tactic) invest more in accessory glands. This pattern has possibly emerged because these organs also function to optimize sperm economy and sometimes also play a role in parental care, which provides more benefits to guarder males. To tease apart these contrasting patterns, we examined tactic-specific investment in and histology of accessory glands, as well as the effect of their fluids on sperm performance in guarder males, using the plainfin midshipman fish (Porichthys notatus). We found that midshipman accessory glands consist of two distinct structures: nodes and lobules, differing in organization and secretory characteristics both between structures and male types. Like other fishes with alternative reproductive tactics, guarder males invested more in accessory glands and in lobules specifically compared to opportunistic sneaker males. Fluids from both lobule and nodes increased sperm velocity in guarder males. Moreover, guarder males increased their investment in accessory glands across the breeding season. Our results suggest that accessory glands may have multiple functions and may even play a role in parental care and olfactory signalling. Our study emphasizes the diversity in form and function of accessory glands and highlights the importance of these organs in reproduction.

The brood parasite's guide to inclusive fitness theory.

Hamilton's theory of inclusive fitness provides a framework for understanding the evolution of social behaviour between kin, including parental and alloparental care. Brood parasitism is a reproductive tactic in which parasites exploit the care of other individuals of the same species (conspecific parasitism) or different species (interspecific parasitism) to rear their brood. Here, drawing from examples in birds and social insects, we identify two insights into brood parasitism that stem from inclusive fitness theory. First, the kin structure within nests, or between neighbouring nests, can create a niche space favouring the evolution of conspecific parasitism. For example, low average relatedness within social insect nests can increase selection for reproductive cheats. Likewise, high average relatedness between adjacent nests of some birds can increase a female's tolerance of parasitism by her neighbour. Second, intrabrood conflict will be high in parasitized broods, from the perspective of both parasite and host young, relative to unparasitized broods. We also discuss offspring recognition by hosts as an example of discrimination in a kin-selected social behaviour. We conclude that the inclusive fitness framework is instructive for understanding aspects of brood parasite and host evolution. In turn, brood parasites present some unique opportunities to test the predictions of inclusive fitness theory. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

Comparative analysis of life history traits and trends of abundance in coral reefs of the orange-spotted grouper (Epinephelus coioides) from two regions of the Arabian Gulf

Abstract The orange-spotted grouper Epinephelus coioides is one of the most important commercially exploited fish species in the Arabian Gulf. Studies to establish the basic biological knowledge necessary for sustainable exploitation are few and of limited spatial extent. We carry out a comparative analysis of life history traits of this sequential hermaphrodite and of trends of abundance in coral reefs, northern vs. southern Gulf. We found remarkable differences in sex proportion by length and age, rates of somatic growth, size at maturity and production of gonadic biomass, and no differences in the age composition, mode of growth, timing and duration of spawning, natural mortality rate, and trends of abundance. In the northern Gulf, the reproductive tactics could be diandric protogyny or protandric because males disappear at higher size and later age. In the southern Gulf, the strategy is protogyny, with full predominance of females in early life and full predominance of males in late life. In the northern Gulf, the orange-spotted grouper could exhibit bidirectional sex change. We suggest that fisheries policies should be versatile, consisting of regional-wide as well as local management measures, to account for local differences and regional-wide commonalities in life history traits and trends of abundance.

Individual plasticity in alternative reproductive tactics declines with social experience in male guppies

Understanding causes and consequences of behavioural plasticity is a major focus in animal behaviour studies for its importance to any population's ability to persist under changing environments. However, behavioural plasticity in traits linked to reproduction has received surprisingly limited attention, especially in species exhibiting alternative reproductive tactics (ARTs). In this study, we explored how behavioural plasticity in ARTs varies in response to social conditions in male guppies, Poecilia reticulata, an internally fertilizing fish in which males can switch between two ARTs to achieve matings. Males can either court receptive females using elaborate mating displays (courtship), or attempt forced copulations without prior display or female cooperation (sneaking). Although males have a genetic predisposition to engage predominantly in one tactic over the other, the extent to which social experience shapes individual plasticity in these tactics is unknown. We observed that between-individual variation in mating effort and preferred ARTs was repeatable over time and largely explained by variation in body size and coloration between individuals. Moreover, we showed experimentally that males exposed to social cues rapidly developed a preference towards either sneaking or courting, resulting in a rapid decline in individual plasticity compared to their socially deprived counterparts. These findings accord with the theoretical predictions that behavioural plasticity should decline as individuals incrementally adjust to local environmental conditions and, thus, when environmental uncertainty is reduced.

Alternative reproductive tactics and lifetime reproductive success in a polygynandrous mammal

Alternative reproductive tactics and lifetime reproductive success in a polygynandrous mammal

Daily energy expenditure of males following alternative reproductive tactics: Solitary roamers spend more energy than group-living males

In many species, males follow alternative reproductive tactics (ARTs), where one tactic (called bourgeois) has much higher reproductive success than alternative tactics followed by males with lower competitive ability. The extent to which ARTs differ in energetic costs is unknown, but it is important to understand the fitness payoffs of ARTs. We studied male African striped mice (Rhabdomys pumilio) which follow one of three ARTs: heavy bourgeois males defend harems of females and have 10 times higher reproductive success than smaller roamers, which have ten times higher reproductive success than philopatric males, which remain in their natal group and are the smallest males. Bourgeois and philopatric males live in social groups that defend one territory, while roamers are solitary and roam over larger areas. We predicted that roamers will face higher energetic costs compared to group-living males because they do not gain thermoregulatory benefits of huddling in groups and might travel larger distances as they have larger home ranges. We measured daily energy expenditure (DEE) of 30 males, resting metabolic rate (RMR) of 79 males, travel distances and daily ranges of 31 males and changes in body mass of 51 males. Roamers had higher DEE and higher RMR than both types of group-living males. Philopatric males had shorter travel distances and smaller daily ranges than both roamers and bourgeois males, which did not differ from each other. This indicates that the higher DEE of roamers compared to bourgeois males cannot be explained by larger travel distances. Philopatrics gained body mass faster than bourgeois males and roamers, thereby increasing their competitive ability and thus the probability of later switching to a tactic of higher reproductive success. Our results suggest that roamers suffer energetic costs that might reduce their ability of gaining body mass and thus the likelihood of switching to the bourgeois tactic, indicating evolutionary trade-offs between investing energy into roaming versus gaining body mass.

Recruitment variation disrupts the stability of alternative life histories in an exploited salmon population.

Males of many fish species exhibit alternative reproductive tactics, which can influence the maturation schedules, fishery productivity, and resilience to harvest of exploited populations. While alternative mating phenotypes can persist in stable equilibria through frequency‐dependent selection, shifts in tactic frequencies have been observed and can have substantial consequences for fisheries. Here, we examine the dynamics of precocious sneaker males called “jacks” in a population of sockeye salmon (Oncorhynchus nerka) from Frazer Lake, Alaska. Jacks, which are of little commercial value due to their small body sizes, have recently been observed at unusually high levels in this stock, degrading the value of regional fisheries. To inform future strategies for managing the prevalence of jacks, we used long‐term monitoring data to identify what regulates the frequencies of alternative male phenotypes in the population over time. Expression of the jack life history could not be explained by environmental factors expected to influence juvenile body condition and maturation probability. Instead, we found a strong positive association between the proportion of individuals maturing as jacks within a cohort and the prevalence of jacks among the males that sired that cohort. Moreover, due to differences in age‐at‐maturity between male phenotypes, and large interannual variability in recruitment strength, jacks from strong year‐classes often spawn among older males from the weaker recruitments of earlier cohorts. Through such “cohort mismatches,” which are amplified by size‐selective harvest on older males, jacks frequently achieve substantial representation in the breeding population, and likely high total fertilizations. The repeated occurrence of these cohort mismatches appears to disrupt the stabilizing influence of frequency‐dependent selection, allowing the prevalence of jacks to exceed what might be expected under equilibrium conditions. These results emphasize that the dynamics of alternative life histories can profoundly influence fishery performance and should be explicitly considered in the management of exploited populations.

Fitness Consequences of Female Alternative Reproductive Tactics in House Mice (Mus musculus domesticus).

Alternative reproductive tactics (ARTs) are defined as discrete differences in morphological, physiological, and/or behavioral traits associated with reproduction that occur within the same sex and population. House mice provide a rare example of ARTs in females, which can rear their young either solitarily or together with one or several other females in a communal nest. We assessed the fitness consequences of communal and solitary breeding in a wild population to understand how the two tactics can be evolutionarily stable. Females switched between the two tactics (with more than 50% of all females having two or more litters using both tactics), pointing toward communal and solitary breeding being two tactics within a single strategy and not two genetically determined strategies. Communal breeding resulted in reduced pup survival and negatively impacted female reproductive success. Older and likely heavier females more often reared their litters solitarily, indicating that females use a condition-dependent strategy. Solitary breeding seems the more successful tactic, and only younger and likely less competitive females might opt for communal nursing, even at the cost of increased pup mortality. This study emphasizes the importance of analyzing phenotypic plasticity and its role in cooperation in the context of female ARTs.

Life-history consequences of bidirectional selection for male morph in a male-dimorphic bulb mite

Intralocus sexual conflict (IASC) arises when males and females have different trait optima. Some males pursue different alternative reproductive tactics (ARTs) with different trait optima, resulting in different strengths of IASC. Consequently, for instance daughter fitness is differentially affected by her sire’s morph. We tested if—and which—other life-history traits correlatively change in bidirectional, artificial selection experiments for ARTs. We used the male-dimorphic bulb mite Rhizoglyphus robini, the males of which are high-fitness ‘fighters’ or low-fitness ‘scramblers’. Twice in each of the five generations of selection, we assessed clutch composition (number of mites of the various life stages present) and size (total number of offspring). Furthermore, we tracked offspring from egg to adulthood in the first and final generation to detect differences between selection lines in the size and duration of stages, and in maturation time. We found that selection for male morph increased the frequency of that morph. Furthermore, compared to fighter lines, scrambler lines produced more females, which laid larger eggs (in the final generations), and maintained a higher egg-laying rate for longer. Otherwise, our results showed no consistent differences between the selection lines in clutch size and composition, life stage size or duration, or maturation time. Though we found few correlated life-history trait changes in response to selection on male morph, the differences in egg laying rate and egg size suggest that IASC between fighters is costlier to females than IASC with scramblers. We hypothesize that these differences in reproductive traits allow fighter-offspring to perform better in small, declining populations but scrambler-offspring to perform better in large, growing populations.

Growth and otolith morphology vary with alternative reproductive tactics and contaminant exposure in the round goby Neogobius melanostomus

Round goby Neogobius melanostomus sagittal (saccular) otolith morphology was compared between males of the two alternative reproductive tactics (termed guarder and sneaker males) and between males captured from sites of high or low contamination. Otolith size increased with fish size and also displayed an ontogenetic shift in shape, becoming relatively taller as otoliths grew in size. Despite a considerable overlap in age between males adopting the two reproductive tactics, size-at-age measurements revealed that guarder males are significantly larger than sneakers at any given age and that they invest more into somatic growth than sneaker males. Controlling for body size, sneaker males possessed heavier sagittal otoliths than guarder males. Subtle otolith shape differences were also found between the two male tactics and between sites of high and low contaminant exposure. Sneaker males had relatively shorter otoliths with more pronounced notching than guarder males. Fish captured at sites of high contamination had otoliths showing slower growth rates in relation to body size and their shapes had more pronounced caudal points and ventral protrusions when compared with fish captured at sites of low contamination. The results are discussed in relation to life-history tradeoffs between the male tactics in terms of reproductive and somatic investment as well as the putative metabolic costs of exposure to contaminants. Overall, this study reveals that male alternative reproductive tactics and environmental contaminants can have small, yet measurable, effects on otolith morphology and these factors should be accounted for in future research when possible.

A costly chemical trait: phenotypic condition dependence of cuticular hydrocarbons in a dung beetle.

Chemical traits are increasingly recognized as important cues used in mate choice. For example, the cuticular hydrocarbons (CHCs) of insects have been shown to influence mating success in a range of taxa. Less is known, however, about how CHCs are expressed in proportion to an individual's condition, and consequently whether CHCs can function as condition-dependent signals of quality. We investigated this question using the dung beetle, Onthophagus taurus. CHCs are subject to sexual selection in this species through mate choice. A dietary manipulation revealed condition dependence of CHC expression for both sexes: dietary restriction decreased overall CHC production and altered the composition of CHCs. Furthermore, CHC production was associated with a measure of condition in beetles fed a limited diet but not those fed adlibitum. These results implicate a resource cost to CHC production that is likely to result in trade-offs with other fitness components in this species, as these respond similarly to a dietary restriction. The CHC profiles showed sexual dimorphism: males produced more CHCs and the sexes differed in the blend of compounds they produced. There was evidence for a male dimorphism in the CHC profile, in line with the presence of the alternative reproductive tactics (minor sneaks and major fighters) in this species. However, rather than mimicking a female CHC profile, minor males differed more from females than major males. Our results suggest that CHCs are a costly trait in O.taurus that has the potential to act as a condition-dependent signal of quality.

An eco-evolutionary feedback loop between population dynamics and fighter expression affects the evolution of alternative reproductive tactics.

Surprisingly, little is known about how eco‐evolutionary feedback loops affect trait dynamics within a single population. Polymorphisms of discrete alternative phenotypes present ideal test beds to investigate this, as the alternative phenotypes typically exhibit contrasting demographic rates mediated through frequency or density dependence, and are thus differentially affected by selection.Alternative reproductive tactics (ARTs), like male fighters and sneakers, are an extreme form of discrete phenotype expression and occur across many taxa. Fighters possess weapons for male–male competition over access to mates, whereas sneakers are defenceless but adopt tactics like female‐mimicking. Because fighters in some species mortally injure conspecifics, this raises the question whether fighter expression can feed back to affect population size and structure, thereby altering the selection gradient and evolutionary dynamics of ART expression in an eco‐evolutionary feedback loop.Here, we investigated how the eco‐evolutionary feedback loop between fighter expression and population size and structure affects the evolution and maintenance of ARTs. We introduced intraspecific killing by fighters in a two‐sex, two‐ART population model parameterized for the male dimorphic bulb mite (Rhizoglyphus robini) that includes life‐history differences between the ARTs and a mating‐probability matrix analogous to the classic hawk–dove game.Using adaptive dynamics, we found that the intraspecific killing by fighters can extend the range of life‐history parameter values under which ARTs evolve, because fighters that kill other fighters decrease fighter fitness. This effect can be nullified when benefits from killing are incorporated, like increased reproduction through increased energy uptake.The eco‐evolutionary feedback effects found here for a dimorphic trait likely also occur in other fitness‐related traits, such as behavioural syndromes, parental care and niche construction traits. Current theoretical advances to model eco‐evolutionary processes, and empirical steps towards unravelling the underlying drivers, pave the way for understanding how selection affects trait evolution in an eco‐evolutionary feedback loop.

Is it the Song or the Singers? Acoustic and Social Experiences Shape Adult Reproductive Tactics and Condition

When sexual signals are perceived during growth and development they can provide information regarding the social conditions likely to be encountered as an adult. Perception of cues related to the presence and density of future mates and potential competitors can result in altered adult phenotypes. Previous studies have shown that adult male Teleogryllus oceanicus field crickets from a Kauai, Hawaii population reared alone and without hearing conspecific song are more phonotactic than those reared with song. These naive males also reduce investment in body size and immunity. Here we examined whether another source of population density information, the presence of other males, affects behavior, size, and immunity. Specifically, we examined satellite behavior as evidenced by strength of phonotaxis, body condition, and immune response in males reared singly and in groups in the presence and absence of conspecific song. Body condition did not vary with rearing density, and immune response did not vary with either acoustic environment or rearing density. Interestingly, group-housed males were more phonotactic than singly-housed males. This pattern was largely driven by the low levels of phonotaxis exhibited by males that were singly-housed in the presence of conspecific song. These findings suggest that males respond to social cues in addition to conspecific song, but that these cues do not necessarily provide concordant information.

Mandible morphology reflects the type of male antagonism in the ant genus Cardiocondyla (Hymenoptera: Formicidae)

The ant genus Cardiocondyla is characterized by wingless, ergatoid males, which in some species replace the typical winged male. Depending on species, ergatoid males engage in lethal fighting for access to sexual females, establish territories within their nests, or are mutually tolerant. Here we investigate, whether the morphology of ergatoid males and in particular the shape of their mandibles reflect phylogeny or male behaviour. In contrast to the worker mandible, which is relatively similar in shape in the ten species examined, mandibles of ergatoid males show a great variation in size and shape not only between the two clades of Cardiocondyla but also among species belonging to Cardiocondyla clade A. This diversity appears to reflect the diverse reproductive tactics of ergatoid males of different species, with extremely long, anteriorly oriented mandibles associated with indirect killing of adult competitors, while particularly short mandibles possibly constitute an adaptation to a tactic in which ergatoid males crush the cuticle of young rivals.

Feeding Rates in the Swordtail Fish Xiphophorus multilineatus: A Model System for Genetic Variation in Nutritional Programming.

A better understanding of the role of appetite regulation in obesity and metabolic disorders requires consideration of both genetic and developmental influences on appetite. Previously we detected genetic differences in responses to nutritional programming (e.g., the permanent influence that nutrition in early life has on the physiological and metabolic states in adults) on a presumed measure of appetite (feeding rate) in the swordtail fish Xiphophorus multilineatus. In this study we validate that feeding rate is a good measure of appetite, by first demonstrating that it is repeatable and correlated with food consumed when controlling for body size. Second, we detected a significant positive correlation between juvenile growth rates and feeding rates measured in adult males, when growth has ceased. In addition, feeding rates explained significant variation in the size of the nuchal hump, a fat deposit that develops after sexual maturity. Finally, we show that the feeding rates of "courter" males were significantly greater than "sneaker" males, alternative reproductive tactics that are influenced by variation in the Mc4r gene on the Y-chromosome. Our results suggest that examining feeding rate in X. multilineatus could provide valuable insights into how nutritional programming influences appetite independently from food intake, as well as insights into the mechanisms that produce the correlation between delayed maturation and faster growth rates of the courter males as compared with the sneaker males that mature early and grow slower in this species.