Allopaternal Care Research Articles

Alloparental care in glassfrogs: males care for unrelated clutches only when associated with their own

Parental care is costly, thus theory predicts that parents should avoid caring for unrelated offspring. However, alloparenting has been reported in many taxa because it may increase the caregiver mating success or offspring survival. We experimentally investigated the existence of allopaternal care in two glassfrog species, Hyalinobatrachium chirripoi and Centrolene peristicta, and discussed possible costs and benefits. Males mated with multiple females and cared for clutches, while continued to call. In the field, we randomly placed unrelated clutches in the territory of males already caring for their clutches and in the territory of non-attending males. Attending males adopted unrelated clutches, whereas non-attending males abandoned their territories. Once males adopted unrelated offspring, they cared for all clutches in a similar frequency and gained new clutches. Alloparenting was context-dependent, as only males already caring for their clutches adopted unrelated ones. We suggest that steroid hormonal levels might mediate the adoption of unrelated offspring by attending males. Additionally, our results suggest that males do not directly discriminate between related and unrelated offspring. Alloparenting has been widely investigated in different vertebrates, except for amphibians. Thus, our study sheds light on the roles of alloparenting for offspring survival and mating success in this group.

First case of male alloparental care in amphibians: tadpole stealing in Darwin’s frogs

ESR Endangered Species Research Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsSpecials ESR 45:331-335 (2021) - DOI: https://doi.org/10.3354/esr01138 NOTE First case of male alloparental care in amphibians: tadpole stealing in Darwin’s frogs Osvaldo Cabeza-Alfaro1, Andrés Valenzuela-Sánchez2,3,4, Mario Alvarado-Rybak2,5, José M. Serrano3,6, Claudio Azat2,* 1Zoológico Nacional, Pio Nono 450, Recoleta, Santiago 8420541, Chile 2Sustainability Research Centre & PhD Programme in Conservation Medicine, Faculty of Life Sciences, Universidad Andres Bello, Republica 440, Santiago 8370251, Chile 3ONG Ranita de Darwin, Ruta T-340 s/n, Valdivia 5090000, Chile 4Instituto de Conservación, Biodiversidad y Territorio, Facultad de Ciencias Forestales y Recursos Naturales, Universidad Austral de Chile, Casilla 567, Valdivia 5110027, Chile 5Núcleo de Ciencias Aplicadas en Ciencias Veterinarias y Agronómicas, Universidad de las Américas, Echaurren 140, Santiago 8370065, Chile 6Museo de Zoología ‘Alfonso L. Herrera’, Departamento Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Circuito Exterior s/n, Ciudad Universitaria, Coyoacán, Mexico City 04510, Mexico *Corresponding author: claudio.azat@unab.cl ABSTRACT: Alloparental care, i.e. care directed at non-descendant offspring, has rarely been described in amphibians. Rhinoderma darwinii is an Endangered and endemic frog of the temperate forests of Chile and Argentina. This species has evolved a unique reproductive strategy whereby males brood their tadpoles within their vocal sacs (known as neomelia). Since 2009, the National Zoo of Chile has developed an ex situ conservation programme for R. darwinii, in which during reproduction, adults are kept in terraria in groups of 2 females with 2 males. In September 2018, one pair engaged in amplexus, with one of the males fertilizing the eggs. Twenty days later, the second male (the alloparent) ingested all of the 8 viable, recently hatched tadpoles, releasing 2 froglets 9 wk later. This unusual behaviour observed in captivity is complemented by observations in the field of male R. darwinii brooding tadpoles of markedly different sizes, possibly reflecting the brooding of tadpoles from different ovipositions. To our knowledge, this is the first documented case of male alloparental care in amphibians and an example of captive breeding programmes contributing important knowledge about the natural history of threatened species. KEY WORDS: Allopaternal care · Rhinoderma darwinii · Neomelia · Cross-fostering · Ex situ conservation · Captive breeding Full text in pdf format Supplementary material PreviousNextCite this article as: Cabeza-Alfaro O, Valenzuela-Sánchez A, Alvarado-Rybak M, Serrano JM, Azat C (2021) First case of male alloparental care in amphibians: tadpole stealing in Darwin’s frogs. Endang Species Res 45:331-335. https://doi.org/10.3354/esr01138 Export citation Mail this link - Contents Mailing Lists - RSS Facebook - Tweet - linkedIn Cited by Published in ESR Vol. 45. Online publication date: August 26, 2021 Print ISSN: 1863-5407; Online ISSN: 1613-4796 Copyright © 2021 Inter-Research.

Short‐term dynamics of nest occupancy in an allopaternal species, the tessellated darter Etheostoma olmstedi

To inquire how male size interacts with alloparental behaviour and mating success in the tessellated darter Etheostoma olmstedi, males were given a choice of nests with or without eggs; subsequent nest occupancy, takeovers and egg deposits were monitored. Subordinate males readily occupied available nests with eggs but were often evicted by dominant males, suggesting that males of all sizes compete for the opportunity to provide allopaternal care in this species.

Large males have a mating advantage in a species of darter with smaller, allopaternal males Etheostoma olmstedi

Abstract Theory suggests that males that are larger than their competitors may have increased mating success, due to both greater competitive ability and increased attractiveness to females. We examined how male mating success varies with male size in the tessellated darter Etheostoma olmstedi. Previous work has shown that large males tend to move around and breed in vacant breeding sites, and consequently provide less care for their eggs, while smaller individuals can be allopaternal, caring for the eggs of other males as well as for their own. We studied female egg deposition in a natural breeding population using artificial breeding sites and in the laboratory, where female choice of spawning site was restricted to two breeding sites tended by two males of different sizes. In both the field and the laboratory, nests tended by larger males were more likely to receive new eggs. Additionally, the mean size of males associated with a nest was positively correlated with both the maximum coverage of eggs at the nest and the number of times new eggs were deposited. We discuss how the increased mating success of larger males, despite their decreased parental care, may help explain allopaternal care in this species.

Competition for territories does not explain allopaternal care in the tessellated darter

Extensive research has focused on understanding the evolution of parental care, with fishes providing important model systems for understanding patterns of variation within and between species. Classic theory predicts that individuals will care for offspring when the fitness benefits through increased offspring survival and growth outweigh the cost to the parents through decreased future reproductive opportunities. Yet, a puzzling observation not explained by this basic theory is the fact that in some species individuals defend and provision unrelated offspring and thus exhibit alloparental care. The tessellated darter, Etheostoma olmstedi, represents one of the first known examples of allopaternal care in fishes. In this species, males often clean and guard eggs fertilized but deserted by other males. Allopaternal care has been argued to occur in the tessellated darter because of competition for a limited number of mating sites where less dominant males accept territories with eggs when other breeding sites are not available. Here, we test this hypothesis using male territory choice experiments. When allowed to choose between two otherwise identical territories either containing eggs fertilized by another male or with no eggs, males spent significantly more time at territories with eggs. This demonstrates that competition for mating territories is not the primary factor explaining the existence of allopaternal care in the tessellated darter. Instead, males of this species may exhibit allopaternal care to dilute predator pressure on their own eggs or because females prefer to mate with males whose territories contain eggs.

Reproductive success in male sunbleak, a recent invasive fish species in the U.K.

The spawning behaviour of male nest guarding sunbleak Leucaspius delineatus, a recent invasive species in southern England, was studied and quantified for the first time. In the absence of physical differences between territorial and non‐territorial males (i.e. colour, size, etc.), the reproductive behaviour of territorial males was analysed and related to reproductive success. The results showed that females preferred high‐courting and highly aggressive males. The initial cue in female mate choice, however, was based on courtship, while aggression was the decisive behavioural trait in influencing mate choice, providing a direct signal of physical condition and ‘paternal competence’. Some males picked nest sites which were subsequently preferred by other males taking over the nest of a previous male (‘communal nest’), with the new territorial male adopting the eggs already present at the nest. It appears that either due to female preference for nests already containing eggs or lower rates of sired egg predation by dilution among unrelated eggs, sunbleak males have adopted the mating strategy of allopaternal care.

A genetic assessment of parentage in a natural population of dollar sunfish (Lepomis marginatus) based on microsatellite markers.

We employ microsatellite markers to assess mating tactics in Lepomis marginatus. Genetic assignments for 1015 progeny in 23 nests indicate that about 95% of the offspring were sired by their respective nest-guardians, a finding consistent with the apparent absence of a brood parasitic morphotype in this species. Allopaternal care was documented in two nests, one resulting from a nest takeover, the other from cuckoldry by an adjoining nest-tender. Clustered de novo mutations also were identified. About 2.5 females (range 1-7) contributed to the offspring pool within a typical nest. Results are compared to those for other Lepomis species.

Egg mimicry and allopaternal care: two mate-attracting tactics by which nesting striped darter ( Etheostoma virgatum ) males enhance reproductive success

In a variety of fish species with paternal care of offspring, females prefer to spawn in nests that already contain eggs. This female preference has been hypothesized to explain egg thievery in male sticklebacks, allopaternal care of eggs in minnows, and the evolution of egg-mimicking body features in male cichlids and darters. Here we employ microsatellite-based parentage analyses to evaluate the reproductive success of striped darter (Etheostoma virgatum) males that appear to utilize two of these functionally related tactics to entice females to spawn in their nests. In an isolated population (Clear Creek, Ky.), we observed that breeding males develop conspicuous white spots on their pectoral fins. If these spots are egg mimics, as we suspect, then this represents the fourth independent evolutionary origin of egg mimicry documented to date in darters, the first based on pigmentation (as opposed to physical structures), and the first in which the egg mimics vary greatly in number among males. From direct counts of microsatellite genotypes in clutches of embryos, at least 3.8 females contributed to the progeny within a typical nest, and females tended to spawn preferentially with males that were larger and displayed more egg-mimic spots. In another population (Hurricane Creek, Tenn.) without egg mimics, the multi-locus genetic data document that allopaternal care is common, especially among the smallest males who sometimes tend nests containing their own as well as an earlier sire's offspring. Thus, these foster males had adopted egg-containing nests and then successfully spawned with subsequent females. Overall, the genetic data on paternity and maternity, in conjunction with field observations, suggest that egg mimicry and allopaternal care are two mate-attracting reproductive tactics employed by striped darter males to exploit female preferences for spawning in nests with 'eggs'.

Isolation and characterization of microsatellite markers from the Hypoptychus dybowskii (Pisces, Gasterosteiformes)

Abstract Hypoptychus dybowskii (Gasterosteiformes) exhibits allopaternal care frequently caused by various types of male reproductive tactics (sneaking, egg desertion and taking over). In order to understand this interesting reproductive system, we isolated microsatellites loci from H. dybowskii. Five microsatellites showed 2–10 alleles and expected heterozygosities ranged from 0.15 to 0.84. These were not significant deviations from Hardy–Weinberg expectations. These results suggest that these novel polymorphic loci should be useful for parentage analysis of H. dybowskii.

Allopaternal Care in the Pygmy Sculpin (Cottus pygmaeus)

Male Pygmy Sculpins (Cottus pygmaeus) were found to abandon nests that contained clutches of eggs, presumably establishing new nests elsewhere. These abandoned nests were readily occupied by new males (allopaternal males) that continued paternal care of existing clutches and usually acquired new clutches. Significantly more eggs were lost to cannibalism when new males acquired nests than when the original males stayed with their own brood. The size of males that abandoned nests did not differ from that of allopaternal males. Female preference for males with nests that already contain eggs may be the selective force for the occurrence of allopaternal care in this species.

Allopaternal care in the redlip blenny

Territorial male Ophioblennius atlanticus atlanticus were found to switch to experimentally deserted nests of other males and adopt their fry. This alloparental care appears to aid in

Allopaternal care in the redlip blenny

Allopaternal care in the redlip blenny

Allopaternal care in the fathead minnow, Pimephales promelas: stepfathers discriminate against their adopted eggs

Some species of fishes with exclusive male parental care exhibit the phenomena of allopaternal care and female preference for males with eggs. In these species, newly reproductive males adopt and care for the eggs of other males, apparently as a part of their mating strategy. Assuming that adoption is adaptive, I would expect males to discriminate between adopted eggs and eggs that they sired themselves. Specifically, I predicted that adopted eggs would receive less care and suffer heavier mortality than sired eggs. I examined the allocation of care and egg survival for adopted and sired eggs in the fathead minnow, Pimephales promelas, and corroborated both predictions.

Allopaternal care in the fathead minnow, Pimephales promelas: females prefer males with eggs

Some species of fishes with exclusive male parental care exhibit the phenomenon of allopaternal care; that is, some males acquire and care for other males' eggs. We conducted a series of experiments to investigate the dynamics and evolution of allopaternal care in one such species, the fathead minnow (Pimephales promelas). In choosing a nest site, a newly reproductive male tended to take over the nest site of a parental male by evicting the resident male, rather than occupy a physically identical empty nest site. The new male generally cared for the old male's eggs, and in most cases, daily egg survival improved under the new male's care. When males were given a choice among unguarded nest sites, they preferred to occupy nest sites already containing eggs. When eggs were randomly assigned to nesting males, females preferred to spawn with males who had eggs in their nest sites. Thus, it appears that female preference for males with eggs led to the evolution of allopaternal care in the fathead minnow.

Allopaternal care in the tessellated darter, Etheostoma olmstedi (Pisces: Percidae)

Large male tessellated darters, Etheostoma olmstedi, defend flat-bottomed rocks, the undersides of which serve as spawning substrates. Because females attach eggs directly onto bare stone, a spawning bout necessarily decreases the surface area available for further breeding at a nest. In apparent response to the female preference of ovipositing on rocks with the most bare surface, fathers abandon nests with their attached offspring to search for rocks with more uncovered surface. Egg abandonment also results after roving fathers intercept and spawn with ripe females and remain at a different rock to care for a new clutch. In essence, large males appear to maximize the number of eggs they fertilize by sequentially monopolizing breeding patches that are temporarily most desirable to females. The costs to a father of abandoning his eggs appear to be low for two reasons: (1) non-territorial males, created by a scarcity of suitable rocks, readily occupy vacant nests, and clean and aerate the abandoned eggs; and (2) after water hardening, eggs are less vulnerable to cannibalism. The maintenance of eggs by nonparental males may be both incidental to scrubbing the ceiling for their own breeding and adaptive in that viable eggs stimulate females to spawn; neither would appear to involve parental investment costs. Thus, allopaternal care in the tessellated darter may have evolved because it is performed in the selfish pursuit of spawning opportunities while entailing little, if any, of the costs normally subsumed within parental investment.

Hormones and Secondary Sex Characters in the Minnow, Hyborhynchus

Previous articleNext article No AccessHormones and Secondary Sex Characters in the Minnow, HyborhynchusL. S. Ramaswami and Arthur D. HaslerL. S. Ramaswami Search for more articles by this author and Arthur D. Hasler Search for more articles by this author PDFPDF PLUS Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by Volume 28, Number 1Jan., 1955 Article DOIhttps://doi.org/10.1086/physzool.28.1.30152180 Views: 2Total views on this site Citations: 12Citations are reported from Crossref Journal History This article was published in Physiological Zoology (1928-1998), which is continued by Physiological and Biochemical Zoology (1999-present). Copyright 1955 The University of ChicagoPDF download Crossref reports the following articles citing this article:Matthew B. Dugas, Nathan R. Franssen, Maya O. Bastille, Ryan A. Martin Morphological correlates of river velocity and reproductive development in an ornamented stream fish, Evolutionary Ecology 30, no.11 (Aug 2015): 21–33.https://doi.org/10.1007/s10682-015-9790-7Stephanie C. McMillan, Zhe T. Xu, Jing Zhang, Cathleen Teh, Vladimir Korzh, Vance L. Trudeau, Marie-Andrée Akimenko Regeneration of breeding tubercles on zebrafish pectoral fins requires androgens and two waves of revascularization, Development 140, no.2121 (Nov 2013): 4323–4334.https://doi.org/10.1242/dev.095992L. M. Unger, R. C. Sargent Allopaternal care in the fathead minnow, Pimephales promelas: females prefer males with eggs, Behavioral Ecology and Sociobiology 23, no.11 (Jul 1988): 27–32.https://doi.org/10.1007/BF00303054David O. Norris Regulation of Male Gonaducts and Sex Accessory Structures, (Jan 1987): 327–354.https://doi.org/10.1007/978-1-4613-1869-9_11Lawrence M. Unger Nest defense by deceit in the fathead minnow, Pimephales promelas, Behavioral Ecology and Sociobiology 13, no.22 (Aug 1983): 125–130.https://doi.org/10.1007/BF00293802N.R. Liley, N.E. Stacey 1 Hormones, Pheromones, and Reproductive Behavior in Fish, (Jan 1983): 1–63.https://doi.org/10.1016/S1546-5098(08)60301-5D. Sasse, W. Pfeiffer, M. Arnold Epidermale Organe am Kopf von Morulius chrysophakedion (Cyprinidae, Ostariophysi, Pisces), Zeitschrift f�r Zellforschung und Mikroskopische Anatomie 103, no.22 (Jan 1970): 218–231.https://doi.org/10.1007/BF00337313S. K. Nayyar, Bangalore I. Sundararaj Response of the seminal vesicles of the hypophysectomized catfish Heteropneustes fossilis (Bloch) to exogenous androgens, estrogen and corticosteroid+, Journal of Fish Biology 2, no.11 (Jan 1970): 69–78.https://doi.org/10.1111/j.1095-8649.1970.tb03260.xH. Gottfried The occurrence and biological significance of steroids in lower vertebrates. A review, Steroids 3, no.22 (Feb 1964): 219–242.https://doi.org/10.1016/0039-128X(64)90080-7G.J. VAN OORDT Male Gonadal Hormones, (Jan 1963): 154–207.https://doi.org/10.1016/B978-0-12-395549-4.50010-7William S. Hoar Hormones and the reproductive behaviour of the male three-spined stickleback (Gasterosteus aculeatus), Animal Behaviour 10, no.3-43-4 (Jul 1962): 247–266.https://doi.org/10.1016/0003-3472(62)90049-0L.S. Ramaswami Endocrinology of reproduction in fish and frog, General and Comparative Endocrinology 1 (Jan 1962): 286–299.https://doi.org/10.1016/0016-6480(62)90099-0