Alternative Reproductive Strategies Research Articles

A dynamic state variable model suggests a stronger effect of age than individual energetic state on reproductive allocation in burying beetles

Evolutionary fitness is determined by how an organism allocates energy, or other limited resources, to reproduction during its lifetime. For iteroparous organisms, two alternative patterns of lifetime reproductive allocation are terminal investment and reproductive restraint. Terminal investment maximizes an individual’s current reproductive output by allocating all available resources to current reproduction at the cost of future reproduction. In contrast, the reproductive restraint strategy allocates the individual’s resources toward future survival and reproductive events. We used dynamic state variable modeling to investigate the conditions under which the burying beetle, Nicrophorus orbicollis, would balance between reproductive restraint and terminal investment over their lifetime. Our model provides a formal extension, specific to burying beetle biology, of the dynamic terminal investment threshold conceptual model. For young females, we show that delayed reproduction and reproductive restraint are the optimal tactic for all individuals except for those in the highest condition. However, as age increases, terminal investment becomes the optimal tactic over an increasingly broader range of individual conditions. Surprisingly, manipulation of a variety of factors, such as survival rate, resource availability, and metabolic costs, causes only minor changes in the general pattern observed. We suggest that in burying beetles, and other similar organisms, age plays a dominant role in determining the pattern of reproductive allocation over a lifetime. Individual energetic condition is important in changing the boundaries between alternative reproductive strategies, but it does not change the overall pattern of dominance of delayed reproduction or reproductive restraint at early ages and dominance of terminal investment with increasing age.

Males conditionally inseminate at three female body locations according to female mating history and female maturity status in a squid.

In some squids, such as those in the family Loliginidae, upon copulation, females receive and store male-delivered sperm capsules, spermatangia, at two different body locations: the buccal membrane and the distal end of the oviduct. This insemination site dimorphism is associated with alternative reproductive strategies. However, in Loliolus sumatrensis, a species of Loliginidae, the females possess three insemination sites: buccal membrane (BM), basal left IV arm (ARM) and lateral head behind the left eye (EYE), therefore we studied such the unusual phenomena. We developed microsatellite markers and genotyped the paternity of each spermatangium on three sites. We found multiple paternity at every single site and simultaneous usage of all three sites by a few males. The seasonal dynamics of a population in the Seto Inland Sea revealed a set priority for the initial use of insemination sites as BM, followed by ARM and then EYE, whereas the maximum number of stored spermatangia was greater in EYE > ARM > BM. Female maturity status was correlated with the usage pattern of insemination sites but not with the number of stored spermatangia at any insemination site. These results suggest that a male squid inseminates at different locations according to female mating history and female maturity status.

Termite females prefer hybrid mating to parthenogenesis when conspecific males are absent

Abstract Parthenogenesis and interspecific mating are alternative reproductive strategies that species have evolved alternative strategies when the opportunity of sexual reproduction is hindered by the natural environment. However, it is still unclear how to make a choice between parthenogenesis and interspecific mating when females are unable to reproduce sexually with males of the same species. This study mainly investigated the reproductive behaviour of female termites in the absence of male termites of the same species. Here, reproductive behaviours of females Reticulitermes aculabialis (Ra♀) were observed when they encountered a male R. flaviceps (Rf♂) with the absence of male R. aculabialis(Ra♂). The results showed that Ra♀‐Rf♂ tandems were more prevalent and stable compared to Ra♀‐Ra♀ tandems. When a tandem inadvertently broke apart, the female R. aculabialis displayed longer pauses while waiting for male R. flaviceps, but shorter pauses when another female R. aculabialis was involved. Furthermore, there were mating behaviour between female R. aculabialis and males R. flaviceps, resulting in offspring produced in paired Ra♀‐Rf♂ colonies were hybridization between female R. aculabialis and male R. flaviceps. These results suggest that interspecific mating and recombination is an important aspect for the choice of reproduction strategy, which will provide new insights into the trade‐off between gene contribution rate and genetic diversity.

Genomic basis of Y-linked dwarfism in cichlids pursuing alternative reproductive tactics.

Sexually antagonistic selection, which favours different optima in males and females, is predicted to play an important role in the evolution of sex chromosomes. Body size is a sexually antagonistic trait in the shell-brooding cichlid fish Lamprologous callipterus, as "bourgeois" males must be large enough to carry empty snail shells to build nests whereas females must be small enough to fit into shells for breeding. In this species, there is also a second male morph: smaller "dwarf" males employ an alternative reproductive strategy by wriggling past spawning females into shells to fertilize eggs. L.callipterus male morphology is passed strictly from father to son, suggesting Y-linkage. However, sex chromosomes had not been previously identified in this species, and the genomic basis of size dimorphism was unknown. Here we used whole-genome sequencing to identify a 2.4-Mb sex-linked region on scaffold_23 with reduced coverage and single nucleotide polymorphism density in both male morphs compared to females. Within this sex region, distinct Y-haplotypes delineate the two male morphs, and candidate genes for body size (GHRHR, a known dwarfism gene) and sex determination (ADCYAP1R1) are in high linkage disequilibrium. Because differences in body size between females and males are under strong selection in L.callipterus, we hypothesize that sexual antagonism over body size initiated early events in sex chromosome evolution, followed by Y divergence to give rise to bourgeois and dwarf male reproductive strategies. Our results are consistent with the hypothesis that sexually antagonistic traits should be linked to young sex chromosomes.

Immunoecology of Species with Alternative Reproductive Tactics and Strategies

Alternative reproductive tactics and strategies (ARTS) refer to polymorphic reproductive behaviours in which in addition to the usual two sexes, there are one or more alternative morphs, usually male, that have evolved the ability to circumvent direct intra-sexual competition. Each morph has its own morphological, ecological, developmental, behavioural, life-history, and physiological profile that shifts the balance between reproduction and self-maintenance, one aspect being immunity. Immunoecological work on species with ARTS, which is the topic of this review, is particularly interesting because the alternative morphs make it possible to separate the effects of sex per se from other factors that in other species are inextricably linked with sex. We first summarize the evolution, development, and maintenance of ARTS. We then review immunoecological hypotheses relevant to species with ARTS, dividing them into physiological, life-history, and ecological hypotheses. In context of these hypotheses, we critically review in detail all immunoecological studies we could find on species with ARTS. Several interesting patterns emerge. Oddly, there is a paucity of studies on insects, despite the many benefits that arise from working with insects: larger sample sizes, simple immune systems, and countless forms of alternative reproductive strategies and tactics. Of all the hypotheses considered, the immunocompetence handicap hypothesis has generated the greatest amount of work, but not necessarily the greatest level of understanding. Unfortunately, it is often used as a general guiding principle rather than a source of explicitly articulated predictions. Other hypotheses are usually considered a posteriori, but perhaps they should take centre stage. Whereas blanket concepts such as “immunocompetence” and “androgens” might be useful to develop a rationale, predictions need to be far more explicitly articulated. Integration so far has been a one-way street, with ecologists delving deeper into physiology, sometimes at the cost of ignoring their organisms’ evolutionary history and ecology. One possible useful framework is to divide ecological and evolutionary factors affecting immunity into those that stimulate the immune system, and those that depress it. Finally, the contributions of genomics to ecology are being increasingly recognized and sometimes applied to species with ARTS, but we must ensure that evolutionary and ecological hypotheses drive the effort, as there is no grandeur in the strict reductionist view of life.

Climate mediates color morph turnover in a species exhibiting alternative reproductive strategies

Sexual selection is considered the primary driver of morph turnover in many color polymorphic taxa, yet the potential for other factors (like climate) to contribute to polymorphism maintenance and evolution remains unclear. Appreciation for a role of environmental conditions in the maintenance and evolution of color polymorphisms has grown in recent years, generating evidence suggesting that color morphs linked to sexual selection may also diverge in climate sensitivity. Focusing on the three color components contributing to the male tree lizard (Urosaurus ornatus) color morphs, I reveal a marked concordance between patterns of turnover over space and time, with a general affinity of orange- and yellow-colored males to hotter, more variable conditions, and blue colored males to wetter, cooler conditions. An assessment of long-term turnover in the blue color component in response to recent climate change over the past 60 years reinforces these findings. Overall, behavioral asymmetries attributed to sexual selection likely expose competing morphs to divergent environmental conditions in heterogeneous habitats, creating opportunity for natural selection to shape climate sensitivities that also drive turnover in morph color composition. Ultimately, these processes may favor stark asymmetries in morph persistence over the coming decades.

Instances of intraspecific nest parasitism in eastern and Rio Grande wild turkeys

AbstractNest parasitism can play an important role in processes regulating population dynamics of both hosts and parasites. Inter‐ and intra‐specific nest parasitism are 2 alternative reproductive strategies observed to occur in about 1% of all bird species. Recently, low productivity in wild turkey (Meleagris gallopavo) populations has resulted in population declines across the southeastern United States. Reproductive output may be influenced by nest parasitism, but the extent of nest parasitism and how it may be related to productivity of wild turkey populations are poorly understood. Herein, we illustrate 6 unreported examples of intraspecific nest parasitism obtained using GPS telemetry data from female wild turkeys in Georgia and Louisiana during 2014−2018. Further, we report 3 occurrences of nest parasitism in Texas using photographic evidence. Our findings suggest that ≥6% of nests are potentially parasitized, and that multiple females may visit and parasitize a single nest. Given recent declines in reproductive output of wild turkeys throughout the southeastern United States, we encourage researchers to continue assessing potential for nest parasitism across wild turkey populations and how this potential may be influenced by predator abundance and activity.

Reproductive behavior and alternative reproductive strategy in the deep-sea snailfish, Careproctus pellucidus

Reproductive behavior and alternative reproductive strategy in the deep-sea snailfish, Careproctus pellucidus

Genetic diversification and life-cycle of the polychaete Capitella spp. from the English Channel: evidence for sympatric cryptic species and alternative reproductive strategies

Polychaetes belonging to the genus Capitella are known to represent a complex of opportunistic cryptic species that dominates the macrobenthos of organically enriched sediments, such as muddy areas particularly rich in sulfide. With the exception of the species, Capitella capitata (Fabricius) from West Greenland, Capitella spp. from the European Atlantic coast have never been accurately characterized both genetically and morphologically and were often reported as capitata in the literature. The life cycle of these European worms has not been described properly either, despite their widespread use as bio-indicators in ecological studies. The present study provides the first morphological description of Capitella specimens collected along the Brittany coast and the English Channel up to the entrance of the North Sea and their genetic diversification in this region. Both morphological and molecular data are congruent and support the co-occurrence of cryptic species at the tip of Brittany. The most frequent French mt lineages, C-Channel1, C-Atlantic and C-Channel2, although well distinct from Capitella teleta, are also divergent but closer to C. capitata initially described from Greenland. Following barcoding, the most abundant species (C-Channel1) was isolated and reared in the laboratory to describe its life cycle and predict both its dispersal ability and ecological success in the face of the sulfidic muddy habitats of the French harbors.

Birds of different morphs use slightly different strategies to achieve similar reproductive performance following heatwave exposure.

Responses to extreme climatic events may differ between individuals of distinct morphs which differ in life-history strategies, resulting in climate change 'winners' and 'losers' within species. We examined the reproductive performance and carry-over effects on offspring of black- and red-headed Gouldian finches Erythrura gouldiae after exposure to simulated heatwaves of moderate or severe intensity. We expected black-headed pairs' reproductive performance to decline after the severe heatwave because only the condition of black-headed females deteriorates during such a heatwave. Supporting the fact that Gouldian finches of different morphs use alternative reproductive strategies, we found that black-headed females initiated egg-laying a month earlier than red-headed females after experiencing a severe heatwave. We also found that this severe heatwave resulted in shorter spermatozoa in males irrespective of their morph. Despite these effects associated with heatwave intensity, the overall reproductive performance of both morphs was not affected by this factor, which was possibly due to an increased nestling provisioning rate by parents after exposure to the severe heatwave. However, offspring still bore the cost of parental exposure to the severe heatwave, as they showed a reduced condition (lower plasma antioxidant capacity and transient lower breathing rate) and higher oxidative damage (at least in fledglings with black-headed parents). These results suggest that inter-morph phenotypic variability in the Gouldian finch does not result in clear differences in reproductive performance following heatwave exposure, despite basal phenotypic differences between morphs. Whether animals using alternative reproductive strategies are, in the end, differently affected by climate changes will likely depend on the capacity of their offspring to recover from altered developmental conditions.

Pedigree simulations reveal that maternity assignment is reliable in populations with conspecific brood parasitism, incomplete parental sampling and kin structure

Modern genetic parentage methods reveal that alternative reproductive strategies are common in both males and females. Under ideal conditions, genetic methods accurately connect the parents to offspring produced by extra-pair matings or conspecific brood parasitism. However, some breeding systems and sampling scenarios present significant complications for accurate parentage assignment. We used simulated genetic pedigrees to assess the reliability of parentage assignment for a series of challenging sampling regimes that reflect realistic conditions for many brood-parasitic birds: absence of genetic samples from sires, absence of samples from brood parasites and female kin-structured populations. Using 18microsatellite markers and empirical allele frequencies from two populations of a conspecific brood parasite, the wood duck (Aix sponsa), we simulated brood parasitism and determined maternity using two widely used programs, cervus and colony. Errors in assignment were generally modest for most sampling scenarios but differed by program: cervus suffered from false assignment of parasitic offspring, whereas colony sometimes failed to assign offspring to their known mothers. Notably, colony was able to accurately infer unsampled parents. Reducing the number of markers (nine loci rather than 18) caused the assignment error to slightly worsen with colony but balloon with cervus. One potential error with important biological implications was rare in all cases-few nesting females were incorrectly excluded as the mother of their own offspring, an error that could falsely indicate brood parasitism. We consider the implications of our findings for both a retrospective assessment of previous studies and suggestions for best practices for future studies.

Alternative reproductive strategies provide a flexible mechanism for assuring mating success in the European badgers (Meles meles): An investigation from hormonal measures

Selection-pressures differ with population density, but few studies investigate how this can affect reproductive physiology. European badger (Meles meles) density varies from solitary to group-living across their range, with reported mating periods throughout the entire year to specific seasonal periods. Badger reproduction is evolutionarily distinct, interrupting the direct progression from conception to gestation with delayed implantation (DI), allowing for superfecundation (SF). To establish the tactical mating flexibility afforded by DI*SF, we used cross-sectional population-level seasonal variation of circulating sex-steroids for 97 females from a high-density population. Oestradiol was highest in spring among non-parous females, then lower in summer, and remained low during following seasons, suggesting that the mating period was restricted to just spring. Oestrone was consistently higher than oestradiol; it was elevated in spring, lowest during summer, peaked in autumn, and remained elevated for pregnant females in winter. This suggests that oestrone sustains pre-implanted blastocysts throughout DI. Progesterone was low throughout, except during winter pregnancy, associated with implantation and luteal development. In contrast to multiple mating periods reported by lower-density studies, our oestradiol data suggest that, at high-density, females exhibit only one mating period (congruent with testosterone patterns in males studied previously in this same population). While additional mating periods during DI enhance fertility assurance at low-density, at high-density, we propose that when coitus is frequent, fertilisation is assured, precluding the need for further cycles and associated mating risks. This endocrinologically flexible DI*SF mating strategy likely represents a form of balancing selection, allowing badgers to succeed at a range of regional densities.

Viability, behavior, and color expression in the offspring of matings between common wall lizard Podarcis muralis color morphs.

Color polymorphisms are widely studied to identify the mechanisms responsible for the origin and maintenance of phenotypic variability in nature. Two of the mechanisms of balancing selection currently thought to explain the long-term persistence of polymorphisms are the evolution of alternative phenotypic optima through correlational selection on suites of traits including color and heterosis. Both of these mechanisms can generate differences in offspring viability and fitness arising from different morph combinations. Here, we examined the effect of parental morph combination on fertilization success, embryonic viability, newborn quality, antipredator, and foraging behavior, as well as inter-annual survival by conducting controlled matings in a polymorphic lacertid Podarcis muralis, where color morphs are frequently assumed to reflect alternative phenotypic optima (e.g., alternative reproductive strategies). Juveniles were kept in outdoor tubs for a year in order to study inter-annual growth, survival, and morph inheritance. In agreement with a previous genome-wide association analysis, morph frequencies in the year-old juveniles matched the frequencies expected if orange and yellow expressions depended on recessive homozygosity at 2 separate loci. Our findings also agree with previous literature reporting higher reproductive output of heavy females and the higher overall viability of heavy newborn lizards, but we found no evidence for the existence of alternative breeding investment strategies in female morphs, or morph-combination effects on offspring viability and behavior. We conclude that inter-morph breeding remains entirely viable and genetic incompatibilities are of little significance for the maintenance of discrete color morphs in P. muralis from the Pyrenees.

Divergent Gene Expression Following Duplication of Meiotic Genes in the Stick Insect Clitarchus hookeri

Some animal groups, such as stick insects (Phasmatodea), have repeatedly evolved alternative reproductive strategies, including parthenogenesis. Genomic studies have found modification of the genes underlying meiosis exists in some of these animals. Here we examine the evolution of copy number, evolutionary rate and gene expression in candidate meiotic genes of the New Zealand geographic parthenogenetic stick insect Clitarchus hookeri. We characterised 101 genes from a de novo transcriptome assembly from female and male gonads that have homology with meiotic genes from other arthropods. For each gene we determined copy number, the pattern of gene duplication relative to other arthropod orthologues and the potential for meiosis-specific expression. There are five genes duplicated in C. hookeri, including one also duplicated in the stick insect Timema cristinae, that are not or uncommonly duplicated in other arthropods. These included two sister chromatid cohesion associated genes (SA2 and SCC2), a recombination gene (HOP1), an RNA-silencing gene (AGO2) and a cell cycle regulation gene (WEE1). Interestingly, WEE1 and SA2 are also duplicated in the cyclical parthenogenetic aphid Acyrthosiphon pisum and Daphnia duplex, respectively, indicating possible roles in the evolution of reproductive mode. Three of these genes (SA2, SCC2 and WEE1) have one copy displaying gonad-specific expression and all genes, with the exception of WEE1, have significantly different non-synonymous/synonymous ratios between the gene duplicates, indicative of a shift in evolutionary constraints following duplication. These results suggest that stick insects may have evolved genes with novel functions in gamete production by gene duplication.

Social organization and the evolution of life-history traits in two queen morphs of the ant Temnothorax rugatulus.

During the evolution of social insects, not only did life-history traits diverge, with queens becoming highly fecund and long lived compared with their sterile workers, but also individual traits lost their importance compared with colony-level traits. In solitary animals, fecundity is largely influenced by female size, whereas in eusocial insects, colony size and queen number can affect the egg-laying rate. Here, we focused on the ant Temnothorax rugatulus, which exhibits two queen morphs varying in size and reproductive strategy, correlating with their colony's social organization. We experimentally tested the influence of social structure, colony and body size on queen fecundity and investigated links between body size, metabolic rate and survival under paraquat-induced oxidative stress. To gain insight into the molecular physiology underlying the alternative reproductive strategies, we analysed fat body transcriptomes. Per-queen egg production was lower in polygynous colonies when fecundity was limited by worker care. Colony size was a determinant of fecundity rather than body size or queen number, highlighting the super-organismal properties of these societies. The smaller microgynes were more frequently fed by workers and exhibited an increase in metabolic activity, yet they were similarly resistant to oxidative stress. Small queens differentially expressed metabolic genes in the fat body, indicating that shifts in molecular physiology and resource availability allow microgyne queens to compensate for their small size with a more active metabolism without paying increased mortality costs. We provide novel insights into how life-history traits and their associations were modified during social evolution and adapted to queen reproductive strategies.

Extra‐pair paternity, intraspecific brood parasitism, quasi‐parasitism and polygamy in the Red‐footed Falcon (Falco vespertinus)

Based on the genotyping of 97 chicks and 74 adults from 37 families we describe extra‐pair paternity (EPP), intraspecific brood parasitism (IBP), quasi‐parasitism (QP) and polygamy in the Red‐footed Falcon Falco vespertinus. The frequency of chicks resulting from EPP was 2.06% affecting 2.70% of families (two chicks, one nest), the values for IBP were 1.03% and 2.70% for offspring and families, and the same values were detected for QP (each one chick in one nest). Altogether, 4.12% of offspring and 8.11% of families were affected by some of the alternative reproductive strategies. As far as we know, this is the first described case of QP in the genus Falco.

Evidence of alternative reproduction by drifting workers in the Japanese paper wasp, Polistes rothneyi Cameron, 1900 (Hymenoptera: Vespidae)

AbstractIntercolony drifting of the Japanese paper wasp, Polistes rothneyi Cameron, was observed using individual color marking of workers. No genetic relatedness was found by using microsatellite markers between drifting workers and the recipient colony. Genetic analysis of brood in the recipient colony revealed reproduction by non‐kin drifting worker(s) in the queenless host colony. The non‐kin broods were raised like broods of the recipient colony until the genetic analysis. This study is the first evidence of male production by non‐kin workers in temperate eusocial wasps. This natural event would compensate for fitness loss as an alternative reproductive strategy evolved under predation and climatic pressures, and is also discussed from the viewpoint of mutual help.

Baffling: a condition-dependent alternative mate attraction strategy using self-made tools in tree crickets.

Intense sexual selection in the form of mate choice can facilitate the evolution of different alternative reproductive strategies, which can be condition-dependent. Tree cricket males produce long-distance acoustic signals which are used by conspecific females for mate localization and mate choice. Our study shows that baffling, an acoustic call amplification strategy employed by male tree crickets using self-made tools, is a classic example of a condition-dependent alternative strategy. We show that though most males can baffle, less preferred males, such as smaller and lower-amplitude callers, predominantly use this alternative strategy. Baffling allows these males to increase their call amplitude and advertisement range, which attracts a higher number of females. Baffling also gives these males a mating benefit because females mate for longer durations with them. Our results suggest that the advantage of baffling in terms of gain in the number of sperm cells transferred while mating is primarily limited to less preferred males, thus maintaining the polymorphism of calling strategies in the population. We summarize that baffling is a condition-dependent strategy used by less preferred tree cricket males to obtain mating benefits.

Morph-specific seasonal variation of aggressive behaviour in a polymorphic lizard species.

The persistence of colour polymorphism (CP) within a given population is generally associated with the coexistence of alternative reproductive strategies, each one involving specific trade-offs among behavioural, morphological, physiological, and other life histories. Common wall lizard (Podarcis muralis), is a medium-sized diurnal lizard, showing CP in three main colours (yellow, white, and red) on throat and belly, and a morph-specific pattern for both immunocompetence and seasonal variation of T levels. Yellow males show low stamina with high plasma T levels at the beginning of the season, while white males show high stamina with a higher plasma T levels at the end of the season. We hypothesised the presence of two strategies: a risky one, characterised by high aggressiveness played by yellow-morph, and a conservative one by white morph with low aggressiveness. Thus, we tested the aggressive response to conspecifics of yellow and white morphs using a mirror inserted into their cage, mimicking an intrusion of a stranger in their territories, throughout the breeding season (from April to July, 117 trials). We considered three types of aggressive response, with different levels of aggressiveness: (i) bite against the image reflected in the mirror, (ii) seconds spent by the individuals into the half mirrored cage, and (iii) number of times the lizard entered the half mirrored cage. We also considered the number of tongue flicking as explorative behaviour variable. All lizards were tested after a period of acclimatisation to the captivity conditions. Results demonstrate that yellow males showed a higher aggressive response in the early season and a decrease aggressive response towards the end, whereas white males showed an opposite pattern.

Size-dependent male mating tactics and their morphological correlates in Poecilia gillii

Abstract Male alternative reproductive strategies are found in some species of most major animal taxa but are especially widespread in fishes. Mature males of the shortfin molly, Poecilia gillii, display extensive variation in size and morphology. We devised a field test of a priori hypotheses regarding the interrelationships between male size, coloration, morphology and mating tactics. Males did not occur in discrete size classes, but instead occurred in a size and morphological continuum. Large males exhibited darker and more orange-coloured dorsal and caudal fins, whereas small males exhibited lighter and more inconspicuous fin coloration. Furthermore, larger males had proportionately deeper bodies, larger dorsal and caudal fins and shorter gonopodia than smaller males. Our field study of male mating behaviour revealed a lack of courtship in this species, and similar levels of mating attempts (gonopodial thrusts) irrespective of male size. Instead, small males were significantly more likely to chase females than were large males. In contrast, large males exhibited higher rates of gonoporal nibbling (a likely means by which males determine, through chemical factors, whether a female is carrying fertilizable ova) and higher likelihood of chasing other males away. In total, we found evidence for the predicted associations between male size, coloration, morphology and mating behaviour. These associations appear likely to maximize mating success for males of a given body size and phenotype.