We focused on the unique coastal vent ecosystem of Ischia island (Italy), where underwater CO 2 volcanic emissions interact with a seagrass and rocky reef habitat1. CO 2 bubbling from the seafloor drives the seawater pH down to equal to or lower than business-as-usual IPCC projections for 2100 (pH 6.5–7.81,2), effectively creating a “chemical island” approximately 2,000 years old3. Our biological focus is on polychaete worms, as they are an abundant taxonomic group in the vents1. Their consistent vent-dominance and the trends seen in their seasonal abundances indicate the possibility of either multi- and/or transgenerational exposure4,5,6,7. Furthermore, the group exhibits highly diverse reproductive and developmental modes8.

We related the type of early life history strategies employed by species living in the vents with their known distribution and abundances1,5,6. We found twelve of the total thirteen species with known reproductive characteristics colonizing high CO 2 vent areas to be brooding or direct developers (eggs kept in protected maternal environment/no free-swimming larval phases). Ten had higher abundances in the venting areas than in nearby ambient CO 2 areas (Table 1). The exception was one species, morphologically appearing to be Platynereis dumerilii (Audouin & Milne-Edwards, 1834), the only broadcast spawning pelagic developer with higher abundances in the vents5,7,9.

Table 1 Early life-history strategies of all polychaete species present in the lowest pH vent site. Full size table

The observation that brooding polychaete species dominate the CO 2 vent areas, along with evidence for physiological and genetic adaptation in vent-inhabiting Platynereis dumerilii6, prompted further examination of this particular species. To determine whether these adaptations have led to reproductive isolation, we attempted to crossbreed Platynereis individuals collected from within the vent sites with those collected from control sites outside the vent sites, in the laboratory.

A male from the control population in the initial stages of transforming into a pelagic, swimming reproductive P. dumerilii was introduced into a container with an immature adult Platynereis sp. from the vent population. Within two hours, the male prompted this vent-originating worm to develop large yellow eggs, likely a pheromone-induced response between the two sexes10. These eggs filled the female body cavity and were five times larger than the average P. dumerilii eggs. The female proceeded to build a complex tube structure consisting of inner microtubes where she deposited large, fertilized eggs that immediately stopped developing (Fig. 1).

Figure 1 a. Initial cross-breeding activity with (top) Platynereis dumerilii male transforming into a pelagic, swimming epitoke full of sperm and (below) the Platynereis massiliensis female developing large yellow yolky eggs, (250 μm in diameter); b. Female inside tube laying and moving 74 eggs into inner brood tubes after 12 h of pairing with the male; c. Close-up of inner-parental mucus tubes holding large yellow eggs. Scale: 0.5 mm. Full size image

We matched the reproductive description of the female’s brooding behaviour to the parent’s genetic identities using a COI barcoding approach (Supplementary Methods). While the COI sequence of the pelagic form was only 0.7% different from the published sequence of P. dumerilii, the brooding form’s sequence was 26% different, indicating that it represents a separate species. Observational results confirm that the female found in the vents is actually Platynereis massiliensis (Moquin-Tandon, 1869), a sibling species of P. dumerilii11. These two sibling species are morphologically indistinguishable as immature adults but are easily discernible upon maturation, having evolved opposing reproduction modes with morphologically different gametes11,12. Platynereis massiliensis are protandric sequential hermaphrodites that first mature as males and fertilize a female partner’s eggs laid inside a brood tube. The female then dies and the male continues ventilating and protecting the developing embryos inside the tube as they develop into young worms11, after which the father changes sex and the process is repeated in the next reproductive event. Platynereis dumerilii have separate sexes and maturation invokes morphological changes allowing the benthic forms to leave their tubes and swarm in a single spawning event in the surface water. Adults swim to the surface, in synchronization with the full moon, in a pheromone-induced search for the opposite sex11,13. They then release their gametes and die. Fertilization occurs in the sea water and the larvae go through a subsequent six-week pelagic phase10.

Our COI analysis provides the first genetic record for P. massiliensis, as well as a genetic template to match previously sequenced individuals from both inside and outside the venting areas to their correct species identity. We did this using published sequence data from Calosi et al. (2013) for P. dumerilii. Results suggest that the vent site is dominated by brooding P. massiliensis (10:1 with P. dumerilii) and the control site is dominated by broadcasting P. dumerilii (15:1 with P. massiliensis), these differences being significant (Χ2: 9.808, p < 0.005). Additionally, we observed several mating pairs successfully producing juveniles inside their maternal tubes from P. massiliensis parents collected exclusively from the vent site.

It is not known what prompted speciation in these two species11. Existing ecological knowledge suggests that they have comparable sizes, habitats and functions and as such are overcoming similar mechanical, chemical and physical constraints11. Additionally, the known species ranges appear to overlap on a large spatial scale: ripe females and adult males of P. massiliensis have been found in the Gulf of Naples (Italy)12, Banyuls-Sur-Mer (France)11, on the Isle of Man coast (British Sea)14, in a Denmark fjord15 and in Norfolk (UK)16. Platynereis dumerilii is also found in these localities, however we are cautious to compare the species’ global distributions from current records, as observations are limited and not confirmed on a molecular basis17. Speciation may have been sympatric in the past (occurring in the same habitat), but the distribution of the brooding P. massiliensis in the localized venting area of this study clearly shows how this species favours this high CO 2 habitat, whereas the sibling broadcasting P. dumerilii species does not. This pattern can be interpreted as a solid example of pH-driven brooding preference18.

Using the local distribution information of these congeners, we revisit the synthesis of life history strategies for the complete vent polychaete community and affirm that each dominant species exhibits parental care by a form of brooding or direct development (Table 1). The most parsimonious mechanism driving this trend appears to be that of the direct physical protection of early life stages from the water conditions19,20,21. Alternatively, or in part, this trend may be attributed to (1) an evolutionarily based selection for phenotypes tolerant to low pH among brooding species, (2) selection of traits associated with brooding; or (3) selection through some other vent characteristics besides low pH conditions. The possibility that these CO 2 -dominating brooding species have selected phenotypes tolerant to low pH is supported by the general ability of polychaetes to rapidly adapt to chronically disturbed habitats8,22. Furthermore, the traits commonly associated with brooders, such as short larval dispersal, continuous reproduction, in part through hermaphroditism and small adult sizes having smaller broods per reproductive event, support respective population’s survival by continuously selecting for fitness to a specific habitat8,23,24. Low pH habitat-based changes may be indirect factors influencing brooding preference as well4,9,25. For instance, habitat complexity and increased algal growth may cause a loss of brooder predators or competitors not as phenotypically plastic to CO 2 stress, such as microbial shifts deterring pelagic larval recruitment26 Alternatively, a greater availability of sheltered habitat-based types of refugia and/or better food resources for brooding interstitial species living in the algae may occur27,28,29,30. The thirteen polycheate species in this study live in the low pH vent habitat and have many of these traits (Table 1), but further investigation of OA-mediated biological and ecological effects on species’ long-term OA tolerance is needed to distinguish the exact mechanisms responsible for low pH brooding dominance31,32.

These possibilities show that brooding and/or direct development may not be solely contingent on water chemistry, however the dominant species in this open ‘chemical island’ CO 2 vent habitat do appear to be adapted to OA conditions in their reproductive and developmental modes. To broaden and further corroborate our evidence on a relationship between species life history strategy and tolerance to an important global change driver such as OA, we found examples in the literature from other polychaete worms, starfish, cowries and oysters, all following parallel adaptive pathways under climate and environmental-related stressors (Table 2). These species have been found inhabiting areas undergoing rapid environmental alterations and appear to have evolved direct development from broadcasting ancestors to enable them to counteract the detrimental effects of continuous disturbances. Many of these examples show species complexes in which broadcast spawning ancestors retain sensitivity to high CO 2 /low pH and other environmental extremes marked by their absence in disturbed sites, while species showing forms of parental care persist in the disturbed area33,34.

Table 2 Review of marine taxa exhibiting climate-related tolerance and greater parental care compared to their congeneric counterparts, respectively. Full size table

This multispecies comparative method substantiates the idea that today’s organisms exhibiting brooding or direct development may be more successful in responding to future OA than their pelagic broadcast spawning counterparts. One important consideration in this proposed response hinges on dispersal capacity and extinction of brooders in the future ocean. Brooding dispersal capacity is theoretically limited by low mobility of the early developmental phases, but existing evidence counter-intuitively indicate high dispersal ability in many brooder species35,36. The “Rockall paradox” reviews examples of such situations, where isolated islands are void of any pelagic broadcast spawning invertebrates. In these cases, it is noted that pelagic spawning parents assume a risk that their offspring will find suitable habitats for survival and reproduction. This strategy potentially presents difficulties, as pelagic larvae may not be able to find, settle and reproduce in distant places35. The possible link of these isolated islands to the “chemical island” of Ischia’s vents may be that pelagic larval settlement and recruitment success in acidified oceans is highly reduced4,5,7,26, supporting the hypothesis of direct developer pH tolerance. On the global scale of OA, pelagic larvae may be searching in vain for a ‘less acidified’ habitat that can retain a viable population base.

Current research on evolution and adaptation to OA is primarily focused on quantifying genetic variability of OA tolerant traits as an indicator of adaptive capacity into the expected future oceanic conditions37,38,39,40. Within this context, brooders may reach extinction far before their pelagic counterparts, as they typically hold lower genetic variability24. However, our evidence points to the opposite pattern. It would be worthwhile to investigate extinction risks of brooding and pelagic-developing species in the context of global OA at different spatial and temporal scales, in an attempt to constrain the effects of both exposure to ongoing global OA and local extreme events. In fact, while brooding-associated traits may be less advantageous under local extreme events, due to dispersal limitation on a short time scale – within a generation, they may actually prove to be more adaptive in a globally disturbed ocean (on a longer time scale: across multiple generations). Our polychaete-based analysis, supported by a selection of other invertebrate taxa, provides compelling comparative evolutionary-relevant evidence that direct developers/brooders may do better in the globally acidifying ocean than their relatives employing broadcast spawning and pelagic larval development. The general principle we present here will be useful to inform our capacity to identify which marine taxa will likely be more tolerant to ocean acidification, largely advancing our predictive ability on the fate of marine biodiversity simply based on an aspect of species’ life history strategies.