Early origin of parental care in Mesozoic carrion beetles

Significance

We report on the unique discovery of Jurassic and Cretaceous carrion beetles (Silphidae) from China and Myanmar, early relatives of one of the most protected of beetle species in North America, and which clearly preserve evidence indicative of complex parental care. This finding represents the earliest evidence of parental care, a behavioral repertoire that is the first step in the development of truly social behavior and one that is intensely studied by ecologists, ethologists, and evolutionary biologists alike. Our fossils clearly span the origins of parent–offspring communication and allow us to provide a robust estimate of the time of origin for this complex behavior.

Abstract

The reconstruction and timing of the early stages of social evolution, such as parental care, in the fossil record is a challenge, as these behaviors often do not leave concrete traces. One of the intensely investigated examples of modern parental care are the modern burying beetles (Silphidae: Nicrophorus), a lineage that includes notable endangered species. Here we report diverse transitional silphids from the Mesozoic of China and Myanmar that provide insights into the origins of parental care. Jurassic silphids from Daohugou, sharing many defining characters of Nicrophorinae, primitively lack stridulatory files significant for parental care communications; although morphologically similar, Early Cretaceous nicrophorines from the Jehol biota possess such files, indicating that a system of parental care had evolved by this early date. More importantly, burying beetles of the genus Nicrophorus have their earliest first record in mid-Cretaceous Burmese amber, and document early evolution of elaborate biparental care and defense of small vertebrate carcasses for their larvae. Parental care in the Early Cretaceous may have originated from competition between silphids and their predators. The rise of the Cretaceous Nicrophorinae implies a biology similar to modern counterparts that typically feed on carcasses of small birds and mammals.

Understanding the early evolution of many complex or ephemeral behaviors is severely hampered by the frequent lack of fossilized traces. Among these behaviors, parental care represents a significant behavioral adaptation in life history traits and, as one of the core levels of arthropod sociality, has a wealth of sociobiological and behavioral ecological theory behind it (1). Parental care has evolved independently numerous times among animals, including various lineages of insects (1, 2), for which one of the notable examples is the famous burying beetle, otherwise so critical to forensic entomology. With fewer than 200 extant species, the family Silphidae are among the largest and most conspicuous of the staphylinoid Coleoptera (3) and comprise two well-defined subfamilies: the Silphinae and the Nicrophorinae, with the latter characterized by the presence of an epistomal sulcus and paired stridulatory files and the former by the absence of such features. Silphid parental care has been intensively studied (4, 5), with several attempts to explain its origin and subsequent evolution (6, 7). Fossil evidence that elucidates the origin and evolutionary history of this phenomenon is, not surprisingly, lacking, although modern-looking silphids have been discovered in the Tertiary (8–10). Recent discoveries in the Middle Jurassic and Early Cretaceous of northeastern China together provide a unique suite of evidence for the timing of origin of parental care in these beetles, and suggest an ancient and long history to this behavioral adaptation among silphids. Furthermore, evidence from olfactory structures preserved in minute detail on the antennae of these fossils reveals them to have already adapted to feeding on carrion, perhaps being important recyclers of small-bodied vertebrates during the Age of Dinosaurs.

The material studied herein includes 44 well-preserved specimens belonging to three distinct groups. The first group, characterized by the absence of abdominal stridulatory files, comprises 37 specimens from the Middle Jurassic Daohugou beds (∼165 Mya) at Daohugou, Ningcheng County, Inner Mongolia of China. The second group, with distinct abdominal stridulatory files as in crown-group nicrophorine silphids, includes five specimens from the Lower Cretaceous Yixian Formation (∼125 Mya) at Huangbanjigou, Beipiao City, Liaoning Province and Liutiaogou, Ningcheng County, Inner Mongolia. The third group, with lamellate apical antennomeres, comprises six individuals preserved in two mid-Cretaceous ambers (∼99 Mya) from northern Myanmar.

Results

All Jurassic and Cretaceous beetles are unambiguously referred to Silphidae, as evidenced by their general habitus, clubbed antennae, large mesoscutellum, truncate elytra, and well-separated mesocoxae (3, 11). The diverse transitional silphids extend the earliest records of the family by about 130 million y, the next oldest record being a compression fossil from the Late Eocene (∼35 Mya) of Florissant, Colorado (9). With a body length ranging from 6.5 to 13.5 mm, these Mesozoic beetles are smaller than extant silphids (usually 12–20 mm long). The beetles are obviously suggestive of modern Nicrophorinae, the subfamily including the burying beetles, which locate and bury vertebrate carrion and use it to feed and care for their brood, sometimes with both mother and father contributing to the parental investment (3). The beetles share with Nicrophorinae the presence of a straight epistomal sulcus, relatively short elytra (Figs. 1 A, D, and E, and 2 A–C), and body shape (Figs. 1 A–E and 2 A–C and Figs. S1–S3). The Mesozoic silphids display three distinct types of antennae: one is gradually widened from the base to the distal antennomere, resembling that of some extant silphines (Figs. 1F and 2E); the second is characterized by the apical three antennomeres being moderately to abruptly clubbed, but not lamellate (Figs. 1G and 2F), a feature suggestive of the modern nicrophorine genus Ptomascopus; and the third is characterized by a strongly clubbed antenna with lamellate apical antennomeres 8–10 (Fig. 3C) as those of the burying beetles Nicrophorus (Fig. 3D) (3). Given the similar morphological characters between the Mesozoic and Recent silphids, the former probably had the same feeding habits as modern ones. In most insects the principal olfactory receptors are located on the antennae, with auxiliary ones on the palpi (12, 13). Two types of sensory organs (or sensilla) are recognizable on the antennal club of the Jurassic silphids (Fig. 4C and Fig. S4 D, G, J, and K), perfectly corresponding to those in extant nicrophorine beetles (14), namely sensilla coelosphaerica (Fig. 4 D and E and Fig. S4 E, H, L, and M) and sensilla basiconica (Fig. S4 F and I). The former type is large, round, pit-like, and located on one side of the apical antennomere along its axis; the latter is smaller, hair-like, and distributed on the other side. The identical olfactory structures indicate that silphids in the Jurassic were already adapted to detecting sulfur-containing volatile organic compounds over long ranges, just as in extant nicrophorines and most silphines (15). Mesozoic silphids thus may have been significant scavengers and important to the breakdown and recycling of carcasses in such ancient ecosystems.

Fig. 1.

Silphids from the Middle Jurassic of Daohugou. (A) 156144a, general habitus. (B) 156145a, part. (C) 156145b, counterpart. (D) 156146a, part. (E) 156147a, part. (F) Enlargement of A, left antenna. (G) Enlargement of D, left antenna. (Scale bars: 2 mm in A–E; 500 μm in F and G.)

Fig. 2.

Nicrophorine silphids from the Early Cretaceous of northeastern China. (A) 156150a, from Huangbanjigou, general habitus. (B) 156151 from Huangbanjigou. (C) 156152a from Liutiaogou. (D) Enlargement of abdominal tergite V of C, showing paired stridulatory files. (E) Enlargement of A, left antenna, mirror-imaged. (F) Enlargement of B, right antenna. (Scale bars: 2 mm in A–C; 200 μm in D; 500 μm in E and F.)

Fig. 3.

Mid-Cretaceous and Recent burying beetles Nicrophorus. (A) 156194, dorsal view. (B) 156195, dorsal view. (C) Enlargement of B, left antenna. (D) Nicrophorus satanas Reitter, dorsal view. (Scale bars: 500 μm in C; 2 mm A, B, and D.)

Fig. 4.

Scanning electron micrographs of stridulatory files and antenna. (A) Detail of stridulatory files of Nicrophorus orbicollis Say, 1825. (B) Stridulatory files of Cretaceous silphid, 156152a (compare with Fig. 2D). (C) Enlargement of apical antennomere of 156148b, showing sensilla coelosphaerica and sensilla basiconica. (D) Enlargement of antennomere of modern Nicrophorus orbicollis Say, showing the pit-like sensilla coelosphaerica. (E) Enlargement of antenna of 156148b, showing detail of sensilla coelosphaerica. (Scale bars: 500 μm in A and B; 50 μm in C; 10 μm in D; 20 μm in E.)

Notably, all Cretaceous silphids studied possess a pair of stridulatory files on abdominal tergite (Figs. 2D and 4B, and Fig. S5 D and E) and Y-shaped gular sutures (Fig. S3 K and L) like those found in Nicrophorinae (Fig. 4A and Fig. S5 A–C), so they are firmly placed in Nicrophorinae. The Cretaceous Nicrophorinae from China with the second type of antennae can be placed in more primitive Ptomascopus, whereas those from Myanmar with the third type are attributed to Nicrophorus. It is probable that the mid-Cretaceous and Recent Nicrophorus were derived from among the Early Cretaceous silphids. Together, the Jurassic and Cretaceous taxa form a grade leading to crown-group Nicrophorinae and spanning the origin of stridulatory structures used in parent–offspring communication (Fig. S6).

Discussion

Evidence of parental care in the fossil record is exceptionally limited, reported mainly in dinosaurs (16–21), ostracod crustaceans (22), and rarely in insects (23). Despite extensive research on the ecology, physiology, and behavior of modern burying beetles, the origin of parental care within Nicrophorinae and broadly across all beetles remains elusive. Burying beetles exploit small vertebrate carcasses (usually rodents or birds) and bury them in soil as a source of nutrition for their larvae (3). The parents care for and feed the young as they grow, a condition necessary for sociality and more famously known in taxa such as bees, ants, and termites (24). The closely allied Ptomascopus are known to possess a simpler, possibly primitive, parental care in which adults guard small carcasses and their young against competition from both flies and predators, but without burying the carcasses (7). Parental care in Silphidae is confined to the subfamily Nicrophorinae and absent in Silphinae, although the latter are also carrion-feeding as larvae and adults. The innovation of stridulatory files in Nicrophorinae for parent–offspring communication and defense (25) seems to be critically linked to the origin of parental care, as inhibition of stridulation affects reproduction drastically in extant Nicrophorus males and affects brood care and survival of offspring in females (26). Our discovery of exquisitely preserved Mesozoic silphids sheds new light on the origin and early evolution of parental care. Although Jurassic silphids resemble Ptomascopus, stridulatory files are clearly absent in all individuals, suggesting that these scavengers did not care for their young, as in modern Silphinae. However, the Early Cretaceous nicrophorines having stridulatory files, including Ptomascopus species, likely shared a similar behavior and biology, possessing a simple form of parental care whereby adults guarded small carcasses, alerting their brood to the presence of predators and defending them as necessary. More significantly, true burying beetles, Nicrophorus, with characteristic body shape and antennae, originated in the mid-Cretaceous, suggesting that they likely provided elaborate biparental care to their offspring, including exploiting small vertebrate carcasses (early birds or mammals) and burying them in soil as a source of nutrition for their larvae. This finding demonstrates that such significant adaptations, behavioral and morphological, associated with considerable parental investment, were already well established in the Cretaceous. Although parental care is widespread across the hyperdiverse Coleoptera and has evolved independently multiple times, this is the earliest documentation of such behavioral adaptations within the clade.

Competition for resources and predation have been hypothesized as ecological factors important to the evolution of parental care (27, 28). Modern nicrophorines encounter intense biotic stress from two sources: competition with blow flies (Diptera: Calliphoridae) for food, and threat of predation, potentially by some derived staphylinine rove beetles (Coleoptera: Staphylinidae) (7, 29). Similar competitive pressures may have triggered the origin of parental care among ancient carrion beetles. Calliphorids and other schizophoran flies are unknown before the Tertiary, and even molecular estimates consider their radiation to have occurred around the K/T boundary (∼65 Mya) (30, 31). Calliphorids were certainly not competitors for vertebrate carcasses during the Mesozoic, and although we cannot exclude the possibility of other extinct lineages serving such an ecological role, such evidence is presently not forthcoming. As for potential predators of silphids, these seem to be in abundance. The related rove beetles (Staphylinidae) have a relatively long evolutionary history extending into the early Jurassic (32). Jurassic staphylinids are well known and diverse, comprising several basal lineages (32, 33). Many of these taxa, with inconspicuous mandibles, were possibly mycophagous or saprophagous, like their modern counterparts. However, there was an apparent radiation of the derived subfamily Staphylininae during the Early Cretaceous (34). Interestingly, a diversity of staphylinines has been recovered from the Yixian Formation and many of them are characterized by very prominent, sharp mandibles (Fig. S6 B and C) and large bodies (Fig. S6 A and D–G), as in predaceous groups today. Potential predators of extant nicrophorine larvae include staphylinine genera such as the Staphylinina Creophilus, Ontholestes, and Platydracus (29); several of the Cretaceous rove beetles (Fig. S7) might have shared this life history, although the known Cretaceous taxa are not closely related to the often carrion-attracted Staphylinina (34). It is possible that the rise of predaceous Staphylininae influenced evolution of coeval silphids, perhaps being critical to the origin of parental investments in stem-group Nicrophorinae. Alternatively, or in addition, some early mammals or birds in the Early Cretaceous might have been predators influencing the evolution of silphid biology (see SI Text, Paleodiversity of Contemporaneous Feathered or Haired Vertebrates).

With the origin of crown Mammalia in the Late Triassic (35), early silphids might have already derived from their staphyliniform ancestors at that time. Mid-Jurassic silphids likely fed on carcasses of small mammals and perhaps even feathered dinosaurs, whereas Cretaceous species likely sought, as in modern nicrophorines (3), small mammals (Fig. S8) or birds. The Daohugou biota and adjacent localities have yielded feathered dinosaurs (36, 37) and some terrestrial mammals, including small-sized eutherians and allotherians (35, 38, 39), but no birds. In contrast, the younger Jehol biota preserves evidence of significant radiations for both early birds and mammals, with at least 39 avian and 15 mammalian species reported (40), and with taxa ranging in body size from dozens of grams to several kilograms (40, 41). In addition, bird feathers are well known from Burmese amber (42). Regardless, the Mesozoic diversity highlights an ancient time of origin for parental investment among carrion beetles, and emphasizes the complex interplay between locating a suitable and specialized food source (carrion) and defending against predation for the evolutionary development of extended parent–offspring interactions and communication (stridulation). It is fascinating that much paleoethology and paleoecology are embodied in the relatively minute remains of otherwise great recyclers during the mid-Mesozoic forests of China, and suggests a familiar ecological role and suite of influences in a foreign ecosystem.

Methods

The material studied here is housed at Nanjing Institute of Geology and Paleontology, Chinese Academy of Sciences. The fossils were prepared using a sharp knife. Photographs were taken using a Zeiss Discovery V20 microscope system, with specimens moistened with 70% (vol/vol) alcohol (Figs. S1 E and I–M, S2 A–D, I, L, and M, and S3 K and L) or dry (remaining figures). Photomicrographs of stridulatory files on abdominal tergite V (Fig. 4 A and B and Fig. S5 B–F) and antennal sensilla (Fig. 4 C and D and Fig. S4) were taken with a LEO1530VP field-emission scanning electron microscope.