Size-assortative Pairing Research Articles

Seasonal variation in cuckoldry rates in the socially monogamous cichlid fish Variabilichromis moorii

Mating patterns in animal populations can respond to environmental conditions and consequently vary across time. To examine this variation in nature, studies must include temporal replicates from the same population. Here, we report temporal variation in genetic parentage in the socially monogamous cichlid Variabilichromis moorii from Lake Tanganyika, using samples of broods and their brood-tending parents that were collected across five field trips from the same study population. The sampled broods were either spawned during the dry season (three field trips) or during the rainy season (two trips). In all seasons, we detected substantial rates of extra-pair paternity, which were ascribed to cuckoldry by bachelor males. Paternity shares of brood-tending males were consistently higher, and the numbers of sires per brood were consistently lower, in broods that were spawned in the dry seasons compared to broods from the rainy seasons. In contrast, the strength of size-assortative pairing in our V. moorii population did not vary temporally. Seasonal fluctuations in environmental conditions, such as water turbidity, are proposed as a mechanism behind variable cuckolder pressure. Our data demonstrate the utility of long-term monitoring to improve our understanding of animal mating patterns.

It’s the time of the season: seasonal variation in sexually conflicted size-assortative pairing

It’s the time of the season: seasonal variation in sexually conflicted size-assortative pairing

Populational Evidence Supports a Monogomous Mating System in Five Species of Snapping Shrimps of the Genus Alpheus (Caridea: Alpheidae).

The objective of this study was to verify if populations of the snapping shrimps Alpheus angulosus, A. bouvieri, A. carlae, A. estuariensis and A. nuttingi from Pernambuco, northeastern Brazil, are monogamous based on population data. If these species are monogamous, then the populations must exhibit: 1) higher frequency of individuals living in pairs; 2) non-random population distribution, i.e., pairs are found more often than expected by chance alone; 3) males paired with females regardless of their reproductive condition; 4) sexual dimorphism regarding body size and chelipeds weaponry little pronounced among paired individuals and 5) size-assortative pairing. Our samplings were carried out in August 2015, February and August 2016 and February 2017, in the intertidal zone, during low spring tides. We captured a total of 2,276 specimens: 300 of A. angulosus, 393 of A. bouvieri, 374 of A. carlae, 403 of A. nuttingi and 806 of A. estuariensis. The key population parameters (indicators 1, 2, 3, 4, 5 above) for the four species strongly suggest that all four undergo monogomous mating. Although our frequency distribution demonstrated a higher tendency to find solitary individuals in A. nuttingi and A. estuariensis, the other studied features agree with the occurrence of monogamy in those populations. Lastly, the sexual differences observed in the chelipeds and the existence of solitary egg-carrying females indicated that monogamy in the five species is not rigid, i.e., heterosexual pairing may not last long, due to possible competition between males for females or refuge.

Observations of life history traits of Typton carneus Holthuis, 1951 (Caridea, Palaemonidae): a poorly known sponge-dwelling shrimp

The objective of this study was to investigate some life history traits of the palaemonid shrimp Typton carneus collected from a reef in northeastern Brazil. Samples of the sponges Amphimedon compressa, A. viridis, Desmapsamma anchorata, Dysidea etheria, Haliclona implexiformis and Tedania ignis were analyzed and shrimps were removed from them. A total of 41 individuals were found in Te. ignis, three in H. implexiformis and one in D. etheria; the latter two sponges are new records of sponge hosts for Ty. carneus. Of the specimens associated with Te. ignis, 24 were males, 10 ovigerous females, six non-ovigerous females and one juvenile male. Fecundity varied between 19 to 56 eggs (37 ± 14) per female, and the mean egg volume was 0.033 ± 0.010 mm³. Eleven heterosexual pairs were obtained. Characteristics of the pairs suggest a monogamous mating system for the studied population, such as: the absence of sexual dimorphism in weaponry and body size and presence of paired non-brooding and brooding females carrying eggs in different development stages; and a sex ratio that does not differ from the expected 1:1. However, the lack of size-assortative pairing as well as the low proportion of pairs, compared to solitary individuals, have been observed in polygamous mating systems.

Proximate mechanisms responsible for random mating by size in the Himalayan toad Duttaphrynus himalayanus

Abstract Exploring the mechanisms that affect mating pattern with respect to body size has implications for understanding the evolution of sexual selection. Theory predicts that the absence of a relationship between female body size and fecundity, unbiased operational sex ratio, and a short breeding season will lead to random mating by body size in anuran amphibians. We tested these predictions in the Himalayan toad Duttaphrynus himalayanus inhabiting southeastern Tibet. Our study did not detect any correlation between female body size and number of eggs laid, nor was there a significant difference in the sex ratio of toads captured from the breeding site. In addition, the toads were reproductive for only a short period, from late April to early May (typical of an explosively breeding species). As expected, we detected a weak but not significant relationship between body size of amplexing males and females. Our results revealed no apparent size-assortative pairing in the study population of the Himalayan toad and may contribute to an increasing body of literature on mating patterns in relation to body size in animals with indeterminate growth.

Continuously choosy males and seasonally faithful females: sex and season differences underlie size-assortative pairing

In monogamous mating systems, pair mates frequently share similar characteristics, such as size or ornamentation, a pattern suggesting mutual mate choice. When pairs persist across multiple seasons, preferences for familiar pair mates can either reinforce or disrupt patterns of assortative pairing. Snapping shrimp (Alpheus angulosus) are socially monogamous shrimp that can be found in size-assortative pairs year-round; both sexes could benefit from pairing with larger individuals. To determine the role of pair mate preferences for either size or established pair mates in size-assortative pairing, we performed simultaneous choice trials to test whether (1) either or both sexes prefer larger pair mates, (2) females prefer males with larger claws, or (3) either or both sexes prefer current pair mates over size-matched unfamiliar potential mates. Males, but not females, preferred larger potential pair mates in both the reproductive and nonreproductive seasons; males also showed more mate-searching behaviour, switching more frequently between choice options than females. Females, but not males, preferred their current pair mate over a novel potential pair mate; females also engaged in more frequent switching between pair mates and novel males, but only during the nonreproductive season. Thus, while both males and females exhibit preferences in pairing, size-assortative pairing in snapping shrimp does not result from mutual mate choice for size, but rather preferences for size in one sex, with size-assortative pairing reinforced by preferences for established pair mates in the other. Furthermore, pairing behaviour may be dynamic, shifting across seasons even in a year-round socially monogamous species.

Female sexual maturity as a determining factor of size-assortative pairing in the protandrous spider Manogea porracea (Araneae, Araneidae)

Protandry occurs when males mature prior to females in the breeding season. There may be a fitness benefit for males if they are able to copulate and defend virgin and more fecund females. Therefore, fitness benefits can be investigated by studying assortative mating during mate guarding of virgin females before and after female sexual maturation. The asynchrony of female development in the protandrous spider Manogea porracea (Araneidae) provides an opportunity to investigate how female sexual maturity (subadult and adult females) influence size-assortative pairing. We investigated size differences between couples composed of males and subadult females, and of males and adult females. We hypothesized that size-assortative pairing is stronger in couples with adult females. Adult females were larger than subadults, but the size of males paired with females from both groups was similar. We found assortative pairing within all couples involving an adult female. However, this pattern was not observed among couples with subadult females. It is possible that the production of sexual pheromones by adult females after their last molt intensifies male intrasexual competition, promoting positive assortative pairing. We discuss the potential mechanisms affecting male mate choice and mate competition during pairings in M. porracea.

Acanthocephalan infection patterns in amphipods: a reappraisal in the light of recently discovered host cryptic diversity

Amphipods are model species in studies of pervasive biological patterns such as sexual selection, size assortative pairing and parasite infection patterns. Cryptic diversity (i.e. morphologically identical but genetically divergent lineages) has recently been detected in several species. Potential effects of such hidden diversity on biological patterns remain unclear, but potentially significant, and beg the question of whether we have missed part of the picture by involuntarily overlooking the occurrence and effects of cryptic diversity on biological patterns documented by previous studies. Here we tested for potential effects of cryptic diversity on parasite infection patterns in amphipod populations and discuss the implications of our results in the context of previously documented host-parasite infection patterns, especially amphipod-acanthocephalan associations. We assessed infection levels (prevalence and abundance) of 3 acanthocephalan species (Pomphorhynchus laevis, P. tereticollis and Polymorphus minutus) among cryptic lineages of the Gammarus pulex/G. fossarum species complex and G. roeseli from sampling sites where they occur in sympatry. We also evaluated potential differences in parasite-induced mortality among host molecular operational taxonomic units (MOTUs)-parasite species combinations. Acanthocephalan prevalence, abundance and parasite-induced mortality varied widely among cryptic MOTUs and parasite species; infection patterns were more variable among MOTUs than sampling sites. Overall, cryptic diversity in amphipods strongly influenced apparent infection levels and parasite-induced mortality. Future research on species with cryptic diversity should account for potential effects on documented biological patterns. Results from previous studies may also need to be reassessed in light of cryptic diversity and its pervasive effects.

Acanthocephalan infection patterns in amphipods: a reappraisal in the light of recently discovered host cryptic diversity.

Amphipods are model species in studies of pervasive biological patterns such as sexual selection, size assortative pairing and parasite infection patterns. Cryptic diversity (i.e. morphologically identical but genetically divergent lineages) has recently been detected in several species. Potential effects of such hidden diversity on biological patterns remain unclear, but potentially significant, and beg the question of whether we have missed part of the picture by involuntarily overlooking the occurrence and effects of cryptic diversity on biological patterns documented by previous studies. Here we tested for potential effects of cryptic diversity on parasite infection patterns in amphipod populations and discuss the implications of our results in the context of previously documented host-parasite infection patterns, especially amphipod-acanthocephalan associations. We assessed infection levels (prevalence and abundance) of 3 acanthocephalan species (Pomphorhynchus laevis, P. tereticollis and Polymorphus minutus) among cryptic lineages of the Gammarus pulex/G. fossarum species complex and G. roeseli from sampling sites where they occur in sympatry. We also evaluated potential differences in parasite-induced mortality among host molecular operational taxonomic units (MOTUs)-parasite species combinations. Acanthocephalan prevalence, abundance and parasite-induced mortality varied widely among cryptic MOTUs and parasite species; infection patterns were more variable among MOTUs than sampling sites. Overall, cryptic diversity in amphipods strongly influenced apparent infection levels and parasite-induced mortality. Future research on species with cryptic diversity should account for potential effects on documented biological patterns. Results from previous studies may also need to be reassessed in light of cryptic diversity and its pervasive effects.

Someone like me: Size-assortative pairing and mating in an Amazonian fish, sailfin tetra Crenuchus spilurus

In the absence of constraints, preference for larger mates is expected to evolve, as larger individuals are typical of higher potential fitness. Large females are often more fecund and carry larger eggs (which result in higher number and better quality of offspring), whereas large males usually have more conspicuous ornaments and are better at defending resources. However, intrasexual competition can constrain the access to larger partners, especially when opportunities for mate takeover abound. Here we investigate the relationship between individual’s size and mate choice in relation to one’s own size and their respective mate’s size using the sailfin tetra, a sexually dimorphic Amazonian fish species. We show that ornaments of larger males are exponentially more conspicuous, and larger females are more fecund and carry larger eggs. Contrary to expectation, neither males nor females associated for longer with the larger of two offered potential mates. Instead, individuals of both genders chose opposite-sex individuals of similar sizes to themselves. Additionally, similar-sized pairs were more likely to spawn than couples with higher size asymmetries. Grounded on field observations, we propose that prudent choice should be particularly important in this system, since courtship is long (often taking several days), which offers opportunities for mate takeover. Intrasexual competition, however, cannot readily explain female choice for similar-sized males. We thus suggest that such preference might be best explained by avoidance of filial cannibalism.

The mating system of the symbiotic pea-crab Dissodactylus crinitichelis (Brachyura, Pinnotheridae): monogamy or promiscuity?

The mating systems of symbiotic crustaceans vary broadly, ranging from monogamy to polygamy to promiscuity. This disparity in mating systems coupled with wide differences in host ecology provides opportunities to study the effect of environmental conditions on the social behavior of marine organisms. In this study, we tested the prediction that symbiotic crustaceans inhabiting relatively large and abundant host species are promiscuous rather than monogamous. The host traits above constraint host monopolization and favor host-switching behaviors by males individuals and, thus, ultimately drive promiscuity as a mating system in symbiotic crustaceans. As a model system we used Dissodactylus crinitichelis, a small ‘pea-crab’ that inhabits the relatively large and abundant sand dollar Encope emarginata. We described the population distribution of D. crinitichelis at two intertidal localities in Sergipe, Brazil, and conducted laboratory experiments to infer the mating system of this species. Dissodactylus crinitichelis inhabit sand dollars as adult heterosexual pairs more frequently than expected by chance alone, but these heterosexual pairs did not exhibit size-assortative pairing. Sexual dimorphism was reversed in D. crinitichelis, with males attaining smaller average body sizes than females but exhibiting more elaborated weaponry (male > female claws). These findings disagree with expectations for monogamous symbiotic crustaceans. Laboratory experiments demonstrated that male and female crabs switch among host individuals rather frequently and heterosexual pairs retrieved from the field did not remain together for long times. Our results argue against social monogamy and in favor of promiscuity in D. crinitichelis. Our study supports the notion that host abundance and large body size (relative to that of symbiotic guests) favor promiscuity in symbiotic crustaceans.

Pair formation, home range, and spatial variation in density, size and social status in blotched foxface Siganus unimaculatus on an Okinawan coral reef.

The present study examined pair formation, spatial pattern of home range and spatial variation in density, size and social status of blotched foxface Siganus unimaculatus (family Siganidae) on an Okinawan coral reef. Of 32 pairs sampled for sexing, 31 (96.9%) were heterosexual and showed size-assortative pairing. Developed ovaries were found in April and July, whereas oocytes were immature in August, September and February. Heterosexual pairing was found in both reproductive and non-reproductive periods. Home range size tended to be positively related to fork length (FL). The degree of home range overlap for same size class pairs was smaller than that for different size class pairs. The intraspecific behavior when two pairs approached each other was categorized as ‘attack,’ ‘agonistic display’ and ‘no interactions,’ and the frequency of agonistic behaviors (“attack” or “agonistic display”) was significantly greater than “no interactions.” Underwater observations at a seagrass bed, a rocky reef flat and a sheltered reef slope revealed that the mean FL was significantly smaller at the sheltered reef slope (4–13 cm) than at the rocky reef flat (>13 cm). No individuals were found in the seagrass bed. Most individuals less than 6 cm FL were solitary, whereas most individuals over 7 cm FL were paired. Density was significantly greater on the sheltered reef slope than on the rocky reef flat.

Overestimation of the strength of size-assortative pairing in taxa with cryptic diversity: a case of Simpson's paradox

Size-assortative pairing is one of the most common pairing patterns observed in nature and it probably occurs in many taxa with cryptic diversity. Observed patterns of size-assortative pairing in natural populations may thus be influenced by the co-occurrence of noninterbreeding cryptic groups of individuals living in sympatry. To quantify this potential bias, we sampled amphipods from the Gammarus pulex/Gammarus fossarum crustacean species complex in rivers containing two sympatric and morphologically cryptic groups, i.e. molecular operational taxonomic units (MOTUs). Within each river, MOTUs did not interbreed and differed in mean body size. We measured the strength of size-assortative pairing both within MOTUs and overall, combining both MOTUs for the analysis to test for potential effects of cryptic diversity on pairing patterns. Owing to body size differences between MOTUs, we expected size assortment to be stronger when combining MOTUs, which could represent a case of Simpson's paradox on measures of size-assortative pairing. In accordance with our predictions, in most rivers, combined-MOTU size-assortative pairing was stronger than within-MOTU size-assortative pairing. Combined-MOTU size-assortative pairing also increased with increasing body size difference between the two sympatric MOTUs. We discuss how such spurious correlations may lead to inferential fallacies when studying potential causes of pairing patterns and their consequences for sexual selection and phenotypic diversification. Previous results from studies measuring mating patterns in species in which cryptic diversity is likely to occur should be reappraised in the light of our findings.

Social monogamy in the crab Planes major, a facultative symbiont of loggerhead sea turtles

Studying how host characteristics and ecology affect the mating systems of symbiotic crustaceans offers an opportunity to understand how ecological factors contribute to the evolution of different animal mating systems. In theory, symbiotic crustaceans should display social monogamy with long-term heterosexual pairing when hosts are relatively small in body size and structurally simple, and when hosts have relatively low abundance in habitats where the risk of mortality for symbionts (e.g., predation) away from hosts is high. We test this prediction in the mating system of the flotsam crab (Planes major) and its facultative association with loggerhead sea turtles (Caretta caretta). First, we found that the overall population and sex distributions were non-random and crabs inhabited host turtles as heterosexual pairs more frequently than expected by chance, which supports the hypothesis that P. major is socially monogamous on C. caretta. Second, we found that male crabs pair with females regardless of their reproductive state, male–female pairs do not display size-assortative pairing, crab body size and host turtle body size are not correlated, and crabs display reverse sexual dimorphism in body size and conventional sexual dimorphism in weaponry. These results do not support the hypothesis that social monogamy in P. major is always long term. Instead, our results suggest that the duration of social monogamy in P. major is likely variable and may involve some degree of host switching and intra-sexual (mostly male–male) competition. Our results were only partially consistent with theoretical considerations for how host characteristics and ecology affect the mating systems of symbiotic crustaceans, and future studies should focus on quantifying the degree and direction of host switching to better understand the factors that affect the duration of monogamous pairing when P. major associates with C. caretta.

Mating patterns of Gammarus lacustris (Amphipoda: Gammaridae) from three populations across a gradient on the Tibetan Plateau

The large-male mating advantage and size-assortative mating are two different size-based patterns which deviate from random mating in Gammarus species. The size-assortative pairing in gammarid amphipods may have arisen for microhabitat segregation, loading constraints, sexual selection, or a combination of them. This study investigated the mating patterns of Gammarus lacustris from three populations along an altitudinal gradient in the northeastern Tibetan plateau. We demonstrated that the species shows a size-related non-random mating pattern. There is a strong sexual size dimorphism (SSD) in G. lacustris, which does not vary along the altitudinal gradient. The ultimate cause of male-biased SSD is likely the stronger selection acting on male than on female body size, either because large males have a higher mating success than smaller males (large male advantage at the highest elevation population), or because they mate with larger females with more fecundity in three populations, or both, which results in size-assortative mating of G. lacustris. Additionally, the loading constraint hypothesis (size-assortative patterns potentially increased their fitness in fast-flowing water) cannot be excluded.

Size-Assortative Pairing and Social Monogamy in a Neotropical Lizard, Anolis limifrons (Squamata: Polychrotidae)

Social monogamy, the formation of stable male-female pairs, is uncommon among reptiles and is particularly rare among squamates, in which only a handful of cases has been reported. Only one case of persistent pair formation has ever been reported in anoles, for Anolis limifrons, at a single site in Costa Rica. Detailed studies of A. limifrons at other sites, however, have not shown evidence of pair formation. I revisited the site where pairing was originally reported to observe pair behavior in this species and to measure morphological traits of paired and unpaired animals. I confirmed that male-female pairs are commonly encountered in the wild, although a smaller proportion of the animals observed in this study were found in pairs than previously reported. I also found evidence for size-assortative pairing; larger males tended to be found with larger females and smaller males were found with smaller females. I did not find any differences in the morphology of paired and unpaired animals. Although social monogamy has not been widely reported in squamates, I suggest that more examples of this phenomenon will be described as the social behaviors of poorly known species are increasingly subject to study.

Size-assortative pairing and discrimination of potential mates by humpback whales in the Hawaiian breeding grounds

Assortative pairing, and its relation to mate choice, has rarely been documented in mammals. Using data collected during 1998–2007, we investigated size-assortative pairing as it relates to discrimination amongst potential mates in humpback whale, Megaptera novaeangliae, dyads in the Hawaiian breeding grounds. Across 67 male–female dyads in which both individuals were measured using underwater videogrammetry, male length was positively correlated with female length. Detailed analyses on the assessment of maturity by comparisons with whaling data revealed that mature-sized females associated almost exclusively with mature-sized males and had a significant preference for large mature-sized males. In contrast, mature-sized males were less discriminating in their associations with females and showed no significant preference for mature-sized females. However, mature-sized males that associated with immature-sized females were significantly smaller than males that associated with mature-sized females. Finally, immature-sized males tended to associate with immature-sized females. The sex differences in size preference by mature whales probably reflect the relatively high costs of mature females mating with small or immature males compared to the lower costs of mature males mating with small or immature females. Body size appears to influence the adoption of alternative mating tactics by males such that smaller mature males avoid the costs of competing for the highest-quality females and instead focus their attentions on smaller females that may or may not be mature. Overall, our results provide the first quantitative evidence of size-assortative pairing and female discrimination amongst potential mates in humpback whales and indeed in any cetacean species.

Size-assortative pairing across three developmental stages in the Zeus bug, Phoreticovelia disparata

The mechanisms underlying size-assortative pairing have received considerable attention. Typically, pairing is assumed to occur at, or just prior to, the adult phase of the life cycle. However, in many invertebrates, males commence associations with juvenile females who are more than a single moult away from sexual maturity. These species are ideal to explore the importance of reproductive and survival benefits as mechanisms driving size-assortative pairing. In the Zeus bug, Phoreticovelia disparata, adult males are found riding on juvenile (fourth and fifth instar) and adult females—a behaviour that is costly for females but has survival benefits for males. Using a combination of field collections and laboratory manipulations, we show that pairing is size-assortative both within and between female age classes and that riding males are smaller than non-riding males. In a series of mating trials, we revealed that males attempt to ride any female but that their riding success is dependent on female age. We also provide the first direct evidence of female resistance to male riding attempts in P. disparata. We propose that size-assortative pairing arises through adaptations that have evolved to minimise the potential costs of sexual conflict. We suggest that the selective pressure on males to maximise survival benefits is sufficiently high that it outweighs the reproductive benefits of discriminating against fourth instar females. Finally, given that female resistance is under direct selection in juvenile females, it is likely to be the main form of selective pressure for adult females.

Pairing and reproductive success in two sympatric species of Hyalella (Crustacea, Amphipoda, Dogielinotidae) from southern Brazil

This study aimed at characterizing pairing and reproductive success in relation to male and female sizes of the sympatric freshwater gammarideans Hyalella pleoacuta and H. castroi from southern Brazil. These amphipods exhibit precopulatory mate guarding, in which a male will carry a potential mate beneath its ventral surface, guarding the female for several days until it molts and lays its eggs. The specimens were collected monthly with nets, from November 2003 to July 2004 in two trout aquaculture ponds at Sítio Vale das Trutas locality, São José dos Ausentes County, southern Brazil. The precopulatory pairs and ovigerous females were identified and separated in the field. In the laboratory, they were measured (cephalothorax length in mm), using a micrometer eyepiece in a stereoscopic microscope. Pairing success was estimated from the proportion of mating males and females related to their respective non-pairing individuals by size classes. Reproductive success was estimated from egg production. The mean cephalothorax length of paired males was larger than that of the unpaired males. For females, however, body size not affect pairing success for either species, because mean cephalothorax length of paired females did not differ significantly from unpaired females. Paired and unpaired males of both species of Hyalella were larger than the females. Positive assortative mating by size was observed in both species; i.e., larger males tended to pair with larger females. Male pairing success increased sharply with size. In both species, reproductive success in males increased with body size; however, the females of intermediate size classes showed greater reproductive success. This result supports the hypothesis that loading constraints play a part in structuring size-assortative pairing in these species.

Unexpected male choosiness for mates in a spider

Sexual selection theory traditionally considers choosiness for mates to be negatively related to intra-sexual competition. Males were classically considered to be the competing, but not the choosy, sex. However, evidence of male choosiness is now accumulating. Male choosiness is expected to increase with an individual's competitive ability, and to decrease as intra-sexual competition increases. However, such predictions have never been tested in field conditions. Here, we explore male mate choice in a spider by studying size-assortative pairing in two natural sites that strongly differ in the level of male-male competition. Unexpectedly, our results demonstrate that mate choice shifts from opportunism to high selectivity as competition between males increases. Males experiencing weak competition did not exhibit size-related mating preferences. By contrast, when competition was intense we found strong size-assortative pairing due to male choice: while larger, more competitive males preferentially paired with larger, more fecund females, smaller males chose smaller females. Thus, we show that mating preferences of males vary with their competitive ability. The distinct preferences exhibited by males of different sizes seem to be an adaptive response to the lower reproductive opportunities arising from increased competition between males.