Monogamy in marine fishes

The formation of long-term pair bonds in marine fish has elicited much empirical study. However, the evolutionary mechanisms involved remain contested and previous theoretical frameworks developed to explain monogamy in birds and mammals are not applicable to many cases of monogamy in marine fish. In this review, we summarise all reported occurrences of social monogamy in marine fish, which has so far been observed in 18 fish families. We test quantitatively the role of ecological and behavioural traits previously suggested to be important for the evolution of monogamy and show that monogamous species occur primarily in the tropics and are associated with coral reef environments in which territory defence and site attachment is facilitated. However, there is little evidence that obligately monogamous species are smaller in body size than species that can adopt a polygynous mating system. We review the evidence pertaining to six hypotheses suggested for the evolution of monogamous pair bonds: (1) biparental care, (2) habitat limitation, (3) low population density/low mate availability/low mobility, (4) increased reproductive efficiency, (5) territory defence, and (6) net benefit of single mate sequestration. We outline predictions and associated empirical tests that can distinguish between these hypotheses, and assess how generally each hypothesis explains monogamy within and between breeding periods for species with different types of territories (i.e. feeding only or feeding and breeding). Hypotheses (1) and (2) have limited applicability to marine fishes, while hypotheses (3)-(5) have little empirical support beyond the species for which they were designed. However, the role of paternal care in promoting monogamous pair bonds is not explicit in these hypotheses, yet paternal care has been reported in more than 70 monogamous marine fish. We show that paternal care may act to increase the likelihood of monogamy in combination with each of the proposed hypotheses through decreased benefits to males from searching for additional mates or increased advantages to females from sequestering a single high-quality mate. Among species defending breeding and feeding territories, the benefits, both within and between reproductive periods, of sequestering a single high-quality mate (hypothesis 6) appear to be the best explanation for socially monogamous pairs. For species without parental care (i.e. holding only feeding territories), territory defence (hypothesis 5) in combination with the benefits of guarding a large mate (hypothesis 6) could potentially explain most instances of monogamy. Empirical studies of marine fishes over the past two decades are therefore slowly changing the view of monogamy from a mating system imposed upon species by environmental constraints to one with direct benefits to both sexes.     

Monogamy in a Hyper-Symbiotic Shrimp

Theory predicts that monogamy is adaptive in resource-specialist symbiotic crustaceans inhabiting relatively small and morphologically simple hosts in tropical environments where predation risk away from hosts is high. We tested this prediction in Pontonia manningi, a hyper-symbiotic shrimp that dwells in the mantle cavity of the Atlantic winged oyster Pteria colymbus that, in turn, infects gorgonians from the genus Pseudopterogorgia in the Caribbean Sea. In agreement with theory, P. manningi were found dwelling as heterosexual pairs in oysters more frequently than expected by chance alone. Males and females also inhabited the same host individual independent of the female gravid condition or of the developmental stage of brooded embryos. While the observations above argue in favor of monogamy in P. manningi, there is evidence to suggest that males of the studied species are moderately promiscuous. That females found living solitary in oysters most often brooded embryos, and that males allocated more to weaponry (major claw size) than females at any given size suggest that males might be roaming among host individuals in search of and, fighting for, receptive females. All available information depicts a rather complex mating system in P. manningi: primarily monogamous but with moderately promiscuous males.     

Re-Evaluating Primate Monogamy

Researchers propose hypotheses for the occurrence of monogamy as a social system in primates based on the assumption that there are a group of primates, including humans, which live exclusively in "nuclear families" and share a similar set of social behaviors. Examining the primates purported to be "monogamous" reveals that they cover a wide range of grouping types, mating patterns, taxonomic groups, and evolutionary grades. While there are a few primate species that do live in small, two-adult groups and share a similar set of social behaviors, the vast majority of the supposed "monogamous" primates, including humans, do not. [monogamy, social systems, evolution, variability in social organization]     

Monogamy on the fast track

Social monogamy has evolved multiple times and is particularly common in birds. It is not well understood why some of these species are continuously and permanently paired while others occasionally 'divorce' (switch partners). Although several hypotheses have been considered, experimental tests are uncommon. Estrildid finches are thought to be permanently paired because being short-lived opportunistic breeders, they cannot afford the time to form a new pair relationship. Here it is shown through a controlled experimental manipulation that zebra finches (Taeniopygia guttata) allowed to remain with their partners to breed again are faster to initiate a clutch (by approx. 3 days) than birds separated from their mates that have to re-pair, supporting the hypothesis that continuous pairing speeds up initiation of reproduction, a benefit of long-term monogamy in a small, short-lived, gregarious species.     

Monogamy and long-term pair bonding in vertebrates

The term 'monogamy' represents a complex of mating systems that has been relalively neglected. Monogamy is generally associated with significant biparental care and is most common among birds. Recent work has addressed such aspects as the evolutionary incentives for (and value of) contributions by the male parent, how the distributions of females and critical nesting resources can promote monogamy, male defense of genetic paternity, the causes of long-term mate-retention in certain species, and the subtle means by which sexual selection operates within basically monogamous systems. New advances in testing genetic relatedness, especially DNA fingerprinting, promise much for the assessment of individual costs and benefits of monogamy.     

Egg transport in lizards

The reproductive tracts of several species of lizards were examined to understand the events assoclated with the transport of discharged oocytes following ovulation. At the onset of the reproductive cycle the regressed ovaries and oviducts appear as inconspicuous structures pressed against the dorsal body wall. As the reproductive cycle progresses, they undergo marked changes in position and size. The oviducts migrate ventrally and surround the growing ovarian oocytes, which move anteriorly where coelomic space is more abundant and eventually press intimately against the infundibulum. When ovulation occurs the ostium is in a remarkably strategic location for directly receiving the ovulated oocytes. The virtual isolation of the ovaries from the general coelom by the encapsulating oviducts, and the intimate association of the pre-ovulatory oocytes with the infundibular ostium do not support the current concept advocating the migration of loose ova following ovulation. An alternative explanation for the “trans-coelomic migratiion of ova” is proposed.     

Monogamy in black vultures: genetic evidence from DNA fingerprinting

Recent research has indicated that avian mating systems maycommonly deviate from monogamy due to extrapair fertilizations(EPFs). Because the majority of avian species have long beenconsidered monogamous, accurate measurement of the frequencyof EPFs in a variety of species is important to enhance understandingof the evolution of avian mating systems. We used DNA fingerprintingto investigate the apparently monogamous mating system of blackvultures (Coragyps airaius) by assaying parentage within severalnuclear families. Monogamy is suggested in black vultures becausemated pairs exhibit long-term pair bonding and year-round association,and share incubation and nestling feeding duties equally. Thirtytwobreeders and 36 nestlings representing 16 complete nuclear familieswere tagged for individual identification and sampled for DNAanalysis using 2 restriction enzymes and 3 probes for hypervariableregions. Putative parents were assigned parentage in all cases.We empirically examined the probability of detecting EPFs bycomparing nestlings' fingerprints to those of a putative parentand another randomly chosen adult. All putative parents couldbe assigned with 95%confidence and all outside adults couldbe similarly excluded. There is therefore no evidence for successfulEPFs in this population, indicating a mating system that doesnot deviate from strict monogamy. The complex social behaviorof black vultures may eliminate the opportunity for EPFs dueto the prohibition of copulations in the presence of relatives.     

Green-blood pigmentation in lizards

The green pigment in the plasma of the scincid lizard genus Prasinohaema is identified as the bile pigment biliverdin. Concentrations of biliverdin in the plasma of P. flavipes, P. prehensicauda and P. virens are 714 ± 79 μmol/1 (mean ± one standard deviation), 1020 ± 624 μmol/1 and 819 ± 89 μmol/1, respectively. These values represent the highest concentration of plasma biliverdin measured for any organism and are the first report of non-pathological biliverdin accumulation in amniotes. We review the literature for fish species with high concentrations of plasma biliverdin and pathological biliverdin accumulation in humans; we find that Prasinohaema species have plasma biliverdin concentrations approximately 1.5–30 times greater than fish species with green blood plasma and 40 times greater than humans with green jaundice.     

Monogamy and sex role reversal in the pipefish Corythoichthys haematopterus

We observed the mating pattern and social behaviour of the pipefish Corythoichthys haematopterus in temperate waters of Japan during three successive breeding seasons. Males cared for a clutch in their brood pouch for 9-19 days until hatching and had several broods in the season with nonbrooding intervals of only 1 or 2 days. The population sex ratio was female biased and some females were always excluded from reproduction. Although males were sometimes courted by unmated females together with their regular partners, they always mated with the latter. The pair bond was maintained until the next season if both members survived. When males lost their partners, they remated with neighbouring unmated females within a few days. In contrast, widowed females remained unmated for a long time. Females had larger home ranges and were more active in courtship displays than males. This pipefish provides the first example of sex role reversal among monogamous syngnathid fish. We suggest that mate guarding by females is a primary proximate factor for maintenance of monogamy in this fish. Copyright 2001 The Association for the Study of Animal Behaviour.     

Models of parent-offspring conflict. I. Monogamy

Theoretical models for Trivers (1974) concept of parent-offspring conflict are examined for species in which the effects of the conflict are felt by full sibs. A rare conflictor gene will spread if (f(m) greater than 1/2(m + 1), where f(m) is the fitness gained by a conflictor relative to a non-conflictor offspring (f(m) greater than 1), and m is the amount of parental investment taken by a conflictor relative to m = 1 for a non-conflictor. The range of m alleles which can spread against the parent optimum decreases as the cost to the parent increases until a point is reached where there is no conflict of evolutionary interests. There would be no polymorphism for conflictor: non-conflictor alleles unless special conditions prevail. The conflictor allele which spreads most rapidly as a rare mutant against the parental optimum is not an evolutionarily stable strategy (ESS). The ESS for parent-offspring conflict in monogamous species has mo = f(mo)/2[df(mo)/dmo]. The analytical solutions are confirmed throughout by simulations.     

Social Monogamy in the Big-Clawed Snapping Shrimp, Alpheus heterochelis

Social monogamy has evolved independently in many taxa, and often involves biparental care of the young. Where it does not, mate guarding and shared territoriality have been invoked as causal factors. We evaluated mate guarding and shared resource defence (a common shelter) as factors that could have led to social monogamy in the snapping shrimp, Alpheus heterochelis. This species is found in male–female pairs that defend a common shelter together. Female receptivity lasts only for a few hours immediately after her periodic moult. Their monogamous pair bond may represent mate guarding or joint defence of a territory. Monogamy in A. heterochelis seems most importantly driven by the cryptic nature of the female's moult cycle. We found that males did not discriminate among females at different intermoult stages for pairing, nor did they modulate their defence of mate and shelter (vs. the risk in finding a new shelter and mate) according to female moult stage. This, together with the short period of female receptivity before her single copulation per cycle, make extended mate guarding the most efficient method for a male to secure a mating opportunity. Comparing eviction rates of paired and unpaired shelter residents by conspecific intruders provided no evidence of enhanced resource defence that would confer a selective advantage to a pair. Male presence during the moult is beneficial for the female, as searching for a male during her soft-bodied receptive phase would put her at mortal risk. Our results show empirically for the first time that guarding may be beneficial, even if males are not able to assess the female's reproductive stage. This extends the theoretical framework for understanding the evolution of social monogamy in taxa without biparental care of young.     

Monogamy and brood parasitism: an unlikely pair

Intensive observation of a population of brood parasitic brown-headed cowbirds (Molothrus ater), including 114 marked birds, demonstrated that monogamy is the prevalent mating system. Analysis of 1280 consort events and 73 copulations showed that nearly all copulations were between a female and the male most often seen with her, even though females had ample opportunities to mate with other males. Although monogamy prevails, some pair bonds do not endure throughout the breeding season. They are more unstable during the early season when resident cowbirds are establishing their social interrelations. This study provides strong evidence that the cowbird's mating system varies geographically, as the only previous study based on observed copulations demonstrated promiscuity. Current hypotheses for the evolution of avian mating systems, when considered in light of the field data presently available, do not fully explain the adaptive significance of monogamy in a parasitic bird.     

Olfactory discrimination in scat-piling lizards

Several lizard species in the Australian scincid genus Egernia havebeen reported to deposit scats in piles. We show that E. striolata,which does produce scat piles, and E. inornata, which does not,can both discriminate their own secretions, on paper substrates, fromthose of unfamiliar conspecifics. This was indicated by elevatedtongue flick rates and more time in contact with the unfamiliarstimulus. This was not just a response to a novel stimulus becausethe secretions from another species (E. stokesii) elicited lowerresponses. When scats were presented, only striolata demonstrateddiscrimination between their own scats and those of unfamiliarconspecifics. This suggests that scats could be used to produceindividual signals, perhaps indicating residence status, in scat-pilingspecies. For striolata the signal from scats became less effectiveas the scats became older, suggesting the need to pile scatsto renew the signal.     

Blood sample collection in lizards

Blood sample collection in lizards is an important technique. This column describes techniques for sample collection from the ventral coccygeal vein and the ventral abdominal vein.