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Genetic evidence for alloparental care and frequent multiple paternity in the brooding sea star (Leptasterias sp.)

DOI:10.1007/s00227-019-3487-3
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Felipe S Barreto at Oregon State University
Felipe S Barreto
Kristofer K. Bauer at Oregon State University
Kristofer K. Bauer
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Echinoderms form an abundant and ecologically important group of marine animals, and they are found in nearly every marine environment, from shallow tropical waters to deep polar benthos and even in the pelagic zone. They exhibit a wide diversity of reproductive strategies that range from broadcasting millions of gametes, with no parental care, to internal brooding of a few embryos for several weeks. While many echinoderm species have become model systems for studies of community ecology, evolutionary genetics, and development biology, very little is known about the distribution of mating and reproductive success in natural populations. In this study, we examined patterns of genetic maternity and paternity in the six-rayed sea star Leptasterias sp., an important predator of many intertidal communities and a species that exhibits maternal care of embryos. We used next-generation sequencing to rapidly develop informative microsatellite markers for this species, and used these markers to genotype 439 juveniles across 15 broods collected from the intertidal in Fogarty Creek, Oregon, USA. Our data show an unambiguous pattern of multiple paternity in all but one clutch examined, with some broods showing some of the highest levels of polyandry reported for a marine invertebrate. Moreover, we detected two cases of mixed maternity in which a female sea star carried another mother’s offspring mixed with her own. Alloparental care by females is rare, and since female Leptasterias do not eat during the 40–60 days brooding period, this expensive behavior may provide a useful system for examining the evolutionary costs and benefits of parental care in dynamic intertidal environments.
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Marine Biology (2019) 166:38
https://doi.org/10.1007/s00227-019-3487-3
ORIGINAL PAPER
Genetic evidence foralloparental care andfrequent multiple paternity
inthebrooding sea star (Leptasterias sp.)
FelipeS.Barreto1· KristoferK.Bauer1
Received: 6 October 2018 / Accepted: 2 February 2019 / Published online: 13 February 2019
© Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
Echinoderms form an abundant and ecologically important group of marine animals, and they are found in nearly every
marine environment, from shallow tropical waters to deep polar benthos and even in the pelagic zone. They exhibit a wide
diversity of reproductive strategies that range from broadcasting millions of gametes, with no parental care, to internal
brooding of a few embryos for several weeks. While many echinoderm species have become model systems for studies of
community ecology, evolutionary genetics, and development biology, very little is known about the distribution of mating
and reproductive success in natural populations. In this study, we examined patterns of genetic maternity and paternity in the
six-rayed sea star Leptasterias sp., an important predator of many intertidal communities and a species that exhibits maternal
care of embryos. We used next-generation sequencing to rapidly develop informative microsatellite markers for this species,
and used these markers to genotype 439 juveniles across 15 broods collected from the intertidal in Fogarty Creek, Oregon,
USA. Our data show an unambiguous pattern of multiple paternity in all but one clutch examined, with some broods show-
ing some of the highest levels of polyandry reported for a marine invertebrate. Moreover, we detected two cases of mixed
maternity in which a female sea star carried another mother’s offspring mixed with her own. Alloparental care by females is
rare, and since female Leptasterias do not eat during the 40–60 days brooding period, this expensive behavior may provide
a useful system for examining the evolutionary costs and benefits of parental care in dynamic intertidal environments.
Introduction
Parental investment in the form of nest guarding or brood-
ing of developing embryos occurs in many aquatic taxa,
besides mammals, including crustaceans (Toonen 2004;
Baggio etal. 2011; Jense and Bentzen 2012), pycnogonids
(Barreto and Avise 2010, 2011; Burris 2011), polychaete
annelids (Wilson 1991; Hess 1993), molluscs (Dupont etal.
2006; Voight and Feldheim 2009), echinoderms (Chenuil
etal. 2004; Gillespie and McClintock 2007), and bony fishes
(Avise and Liu 2010; Coleman and Jones 2011). Species
vary in the modality of care with regards to where embryos
are placed, and in which parent attends to the brood. Postzy-
gotic parental care is widely regarded to be costly to the
attending parent because of energy expenditure, suscepti-
bility to predation, and reduced future mating opportunities
(Royle etal. 2012).
Because of these costs, uniparental care of embryos is
theoretically expected to be performed when the parent has
high confidence in its genetic contribution to the brood or
clutch. Consistent with this prediction, males of some spe-
cies have been shown to adjust parental efforts according
to the level of recognized cuckoldry or female promiscu-
ity (Neff 2003; Mehlis etal. 2010). In certain groups with
prolonged paternal care, such as sea spiders (Pycnogonida;
Barreto and Avise 2008, 2010, 2011) and syngnathid fishes
(McCoy etal. 2001; Jones etal. 2001a), specialized mating
behaviors have allowed males to guarantee genetic paternity
of all progeny they carry. However, in many other species
with paternal care, genetic analyses have revealed striking
patterns of cuckoldry and alloparental care (i.e., care of
embryos unrelated to the guardian). For instance, in most
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Electronic supplementary material The online version of this
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supplementary material, which is available to authorized users.
* Felipe S. Barreto
felipe.barreto@oregonstate.edu
1 Department ofIntegrative Biology, Oregon State University,
Corvallis, OR97331, USA
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... DNA concentrations were in the range of 11-57 ng/ μl, and the DNA samples were diluted 1:10 with molecular grade water for PCR and stored in a -20 °C freezer. Ten microsatellite loci developed by Barreto and Bauer (2019) were selected based on high allelic variation and previously demonstrated Hardy-Weinberg and linkage equilibrium (Table S1, S2). An M13 tail (5′-CAC GAC GTT GTA AAA CGA C-3′) was added to the 5′ end of each locus-specific forward primer. ...
... μl for loci Lepta10,11,14,48,and 49, followed by dilution with 48.5 μl water. Dilution factors were determined by Barreto and Bauer (2019) to result in peaks with 300-10,000 relative fluorescent units. Samples were genotyped via capillary electrophoresis in an ABI 3730 DNA Analyzer. ...
Genetic evidence for multiple dispersal mechanisms in a marine direct developer, Leptasterias sp. (Echinodermata: Asteroidea)
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Quantifying patterns of gene flow is critical for predicting the future resilience of local marine communities. Brooding species may be particularly susceptible to extirpation, as the lack of a pelagic larval phase may limit dispersal capacity and increase the risk of local extinction. Here, we investigate the population genetic structure of Leptasterias sp., a brooding sea star and important intertidal predator. Dispersal in this genus occurs primarily by crawling, but some have suggested that occasional “rafting” events can move individuals long distances. We used microsatellite markers to estimate genotypic variation across six collection sites of varying distances apart along the Oregon coast. We found evidence of strong population structure at the level of capes, and especially high divergence between two sites within Cape Blanco. Although cape-level genetic structure is broadly consistent with isolation-by-distance, additional mechanisms may be required to explain the elevated magnitude of genetic divergence on a finer scale. We propose that a known offshore water jet off Cape Blanco may act as phylogeographic barrier, hindering transport of rafting individuals from neighboring sites. This pattern suggests, indirectly, that rafting may be more important than previously appreciated in generating long-term genetic isolation between nearby sites. Our findings suggest that even for a sessile brooding species, connectivity and genetic structure can vary on a fine spatial scale and may be subject to environmental and oceanographic forces.
View
... Members of the phylum possess a unique set of distinctive morphological characters, including pentaradial symmetry, a water vascular system and a mesodermal calcite skeleton, which enabled them to fill varied marine ecological niches (Smith 2005). Modern species display a wide range of reproductive strategies including forms of advanced parental investment (Gillespie and McClintock 2007; Barreto and Bauer 2019), with brooding of young known to occur in all living classes (Gillespie and McClintock 2007). Brooding is an energetically expensive behaviour but greatly increases the survival rate of offspring (Barreto and Bauer 2019), albeit brooded individuals are usually deprived of the advantages of broad geographical dispersion (Cohen and Johnston 1987). ...
... Modern species display a wide range of reproductive strategies including forms of advanced parental investment (Gillespie and McClintock 2007; Barreto and Bauer 2019), with brooding of young known to occur in all living classes (Gillespie and McClintock 2007). Brooding is an energetically expensive behaviour but greatly increases the survival rate of offspring (Barreto and Bauer 2019), albeit brooded individuals are usually deprived of the advantages of broad geographical dispersion (Cohen and Johnston 1987). It is thus assumed to be the result of a wide range of environmental stresses, such as restricted food availability, high risk of predation or ocean acidification of water (Pearse 1994). ...
The oldest evidence of brooding in a Devonian blastoid reveals the evolution of new reproductive strategies in early echinoderms (Pre-peer reviewed)
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This is the pre-peer reviewed version of the following article: Álvarez-Armada, N., Bauer, J. E., Waters, J. A. and Rahman, I. A. 2023. The oldest evidence of brooding in a Devonian blastoid reveals the evolution of new reproductive strategies in early echinoderms. Papers in Palaeontology, 9, e1493, which has been published in final form at https://doi.org/10.1002/spp2.1493. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions."
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... Leptasterias occur in rocky intertidal and subtidal habitats, typically measure less than 6 cm from ray tip to ray tip (Chia, 1966;Fisher, 1930;Niesen, 1973), and mature around 2 years of age (Menge, 1974). Leptasterias are lecithotrophic and females brood their young underneath their rays until the fully developed juveniles crawl away to disperse (Barreto & Bauer, 2019;Chia, 1966;Menge, 1975). Due to their brooding life history and small size, these sea stars have limited dispersal to new sites. ...
Temporal and spatial variation in population structure among brooding sea stars in the genus Leptasterias
Article
Full-text available
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Temporal genetic studies of low‐dispersing organisms are rare. Marine invertebrates lacking a planktonic larval stage are expected to have lower dispersal, low gene flow, and a higher potential for local adaptation than organisms with planktonic dispersal. Leptasterias is a genus of brooding sea stars containing several cryptic species complexes. Population genetic methods were used to resolve patterns of fine‐scale population structure in central California Leptasterias species using three loci from nuclear and mitochondrial genomes. Historic samples (collected between 1897 and 1998) were compared to contemporary samples (collected between 2008 and 2014) to delineate changes in species distributions in space and time. Phylogenetic analysis of contemporary samples confirmed the presence of a bay‐localized clade and revealed the presence of an additional bay‐localized and previously undescribed clade of Leptasterias. Analysis of contemporary and historic samples indicates two clades are experiencing a constriction in their southern range limit and suggests a decrease in clade‐specific abundance at sites at which they were once prevalent. Historic sampling revealed a dramatically different distribution of diversity along the California coastline compared to contemporary sampling and illustrates the importance of temporal genetic sampling in phylogeographic studies. These samples were collected prior to significant impacts of Sea Star Wasting Disease (SSWD) and represent an in‐depth analysis of genetic structure over 117 years prior to the SSWD‐associated mass die‐off of Leptasterias.
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... Multiple paternity, the fertilization of a clutch of multiple eggs by more than one male, is widespread among invertebrates and vertebrates (Barreto & Bauer, 2019;Hill et al., 2017;Schulze et al., 2018;Wacker et al., 2018;Weber et al., 2018;York & Baird, 2019;Yue et al., 2010). Multiple paternity has been investigated, and often observed, in a diverse array of crabs, including Brachyura (e.g., Majidae (Diesel, 1990;Urbani et al., 1998;Sainte-Marie et al., 2008), Portunidae (Hill, et al., 2017), Ocypodidae (Koga et al., 1993;Baggio et al., 2011;Reaney et al., 2012), Cancridae (Mckeown et al., 2008;Jensen & Bentzen, 2012;Rojas-Hernández et al., 2014), and Pinnotheridae (Jossart et al., 2014)), and Anomura (e.g., Galatheidae (Bailie et al., 2011) and Porcellanidae (Toonen, 2004)). ...
Multiple paternity in the intertidal zone porcelain crab Petrolisthes cinctipes Randall, 1840 (Decapoda: Anomura: Porcellanidae) is a life-history strategy that increases fitness during heat stress
Article
Full-text available
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Multiple paternity is widespread across animal and plant taxa and can increase genetic diversity and enhance fitness, especially in unpredictable environments. A prior study of the intertidal zone porcelain crab, Petrolisthes cinctipes (Randall, 1840), found that most females carried polyandrous broods. We tested the hypothesis that multiple paternity in P. cinctipes enhances fitness through increased average brood tolerance to temperature stress. Embryonic survival of split broods (N = 27) was measured under ambient conditions and following a single one-hour heat shock at 30 °C. Two microsatellite loci were used to genotype embryos and mothers in order to distinguish multiple from single paternity in each brood. Mean overall hatching percentage did not differ between singly and multiply sired broods; however, when exposed to a heat-shock, single-sired broods experienced 11% lower hatching success. Though relative fitness was higher in single-sired broods under non-stressful conditions, extrapolation of our results to conditions where temperatures are at least 30 °C (present-day extremes for the California coast) for > 2 days of the embryonic brood period, multiply sired broods have a relative fitness that is approximately 24 times higher after 15 generations. Maternal quality (size) and the timing of the heat shock relative to developmental timing also influence the brood response to heat shock. Our results suggest that multiple paternity reduces embryo survival variance between ambient and heat-shock conditions and that polyandrous behavior could be an advantage for P. cinctipes in the thermally variable high-intertidal zone. We conclude that multiple paternity is an important strategy for increasing fitness by genetic diversification in organisms that experience severe and unpredictable levels of environmental stress.
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... For instance, multiple species of mouth brooding cichlids have been found to recall mixed broods into their mouths for protection (Kellogg, Markert, Stauffer, & Kocher, 1998;Schaedelin, van Dongen, & Wagner, 2012;Sefc et al., 2012) and mixed maternity has been identified in the clutches of embryos carried on the underside of female six-rayed sea stars Leptasterias spp. (Bareto & Bauer, 2019). ...
Evidence of fostering in an internally brooding sea anemone
Article
Full-text available
Evidence of alloparental care during the incubation stage has largely been demonstrated for species that incubate their offspring externally in a nest. Alloparental care in these species generally consists of the rearing of mixed broods which contain a low proportion of "foreign" young alongside the host's own offspring. However, many animals, including sea anemones, incubate offspring either on or within their bodies. The beadlet anemone Actinia equina incubate their young internally, and as many sea anemones are capable of reproducing both sexually and asexually, the origin of these internally brooded young has been the subject of much debate. While genetically identical young are brooded internally under the juvenile stage, it is thought that those produced sexually are released as larvae into the water and must return to the gastric cavity of an adult in order for metamorphosis to occur. As the likelihood of a planula larva finding its way back to its parent is slim, this suggests that alloparental care may play a role in the survival of juveniles in this species, a hypothesis first suggested a century ago but rarely tested. Here, using highly polymorphic microsatellite markers, we find evidence of alloparental care in A. equina. Our results indicate that while a high proportion of juveniles were genetically identical to their brooding adult, the remaining juveniles showed stark genetic differences to their brooding adult. These juveniles shared far fewer alleles with their "parent" than expected under sexual reproduction, indicating that they were not the adult's offspring. Furthermore, we found variation in the genetic composition of broods, which consisted either of (a) entirely genetically identical individuals, (b) a mix of unique individuals and clonemates or (c) entirely unique individuals, that is no shared genotype. Our results thus indicate that adult A. equina tolerate the presence of non-offspring within their gastric cavity and furthermore that they may incubate entirely "foreign" broods.
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The oldest evidence of brooding in a Devonian blastoid reveals the evolution of new reproductive strategies in early echinoderms
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Brooding of young is a reproductive strategy observed in many extant echinoderms, but the evolutionary history of this behaviour is largely unknown due to the scarcity of examples preserved in the fossil record. Here, synchrotron x‐ray tomography is used to describe an exceptionally preserved specimen of the Devonian blastoid echinoderm Hyperoblastus reimanni . The coelomic cavity appears completely preserved in a coiled arrangement partially enclosing organs associated with the digestive, haemal and axial systems. The vault region of the coelom surrounds four structures interpreted as three internally brooded larvae and a gonad. The presence of putative larvae brooded internally in this specimen sheds new light on the reproductive strategies used by blastoids, suggesting they were sexually dimorphic and that internal brooding was acquired early in the group's history. The acquisition of brooding may have been linked to high clastic sediment influx associated with the Appalachian Orogeny, which would have been detrimental to the survival of larvae living at the soupy sediment–water interface.
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Phylogeography of direct-developing sea stars in the genus Leptasterias in relation to San Francisco Bay outflow in central California
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Effective population sizes with multiple paternity.
Article
While the concept of effective population size is of obvious applicability to many questions in population genetics and conservation biology, its utility has suffered due to a lack of agreement among its various formulations. Often, mathematical formulations for effective sizes apply restrictive assumptions that limit their applicability. Herein, expressions for effective sizes of populations that account for mating tactics, biases in sex ratios, and differential dispersal rates (among other parameters) are developed. Of primary interest is the influence of multiple paternity on the maintenance of genetic variation in a population. In addition to the standard inbreeding and variance effective sizes, intragroup (coancestral) and intergroup effective sizes also are developed. Expressions for effective sizes are developed for the beginning of nonrandom gene exchanges (initial effective sizes), the transition of gene correlations (instantaneous effective sizes), and the steady-state (asymptotic effective size). Results indicate that systems of mating that incorporate more than one male mate per female increase all effective sizes above those expected from polygyny and monogamy. Instantaneous and asymptotic sizes can be expressed relative to the fixation indices. The parameters presented herein can be utilized in models of effective sizes for the study of evolutionary biology and conservation genetics.
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