Same-Sex Sexual Behavior in invertebrates is widespread and context-dependent: insights from a Systematic Synthesis

doi:10.21203/rs.3.rs-7567028/v1

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Same-Sex Sexual Behavior in invertebrates is widespread and context-dependent: insights from a Systematic Synthesis

https://doi.org/10.21203/rs.3.rs-7567028/v1

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Same-sex sexual behavior (SSB) in invertebrates encompasses a wide range of interactions, including courtship, mounting, copulation, and pair bonding between individuals of the same sex. Through a systematic review of 219 primary studies and 12 reviews, we found evidence of SSB in 203 species, spanning arthropods, mollusks, annelids, echinoderms, nematodes, and flatworms. Reports were heavily biased toward insects, which represented nearly 90% of the dataset, reflecting research effort rather than true prevalence. Approximately three quarters of the cases were observed in natural conditions, while the remainder derived from laboratory studies. Male–male copulation and courtship accounted for the majority of reports, but female–female interactions and reciprocal behaviors were also recorded, the last particularly in hermaphroditic taxa. The main explanatory frameworks identified were mistaken identity or indiscriminate mating, social and environmental influences, and adaptive functions. While non-adaptive mechanisms remain a plausible explanation in some contexts, adaptive roles were supported by multiple cases, including enhanced mating practice, reproductive assurance, anti-predator strategies, and stress relief. Fitness consequences were rarely measured directly, but when reported they revealed both costs, such as reduced lifespan or genital injury, and benefits, such as improved reproductive success under biased sex ratios. The synthesis of available evidence suggests that SSB is not an anomaly but a flexible component of reproductive strategies in invertebrates. Rather than being maladaptive, it emerges as context-dependent behavior influenced by ecological and social pressures, and in some cases may confer selective advantages.

invertebrates

behavioral ecology

homosexual behavior

same-sex sexual behavior

Same-sex sexual behavior (SSB), defined as any sexual interaction between individuals of the same sex, has been documented across a broad range of animal taxa, including invertebrates (Bagemihl 1999; Bailey and Zuk 2009). These interactions may involve courtship, mounting, copulation, genital contact, or pair bonding (Bailey and Zuk 2009). Traditionally, sexual behavior in animals has been viewed through a binary, reproduction-focused lens, centered on male-female copulation as the primary route to fitness. This perspective has shaped classical evolutionary theory by linking reproductive success exclusively to heterosexual mating and offspring production. However, growing evidence of SSB challenges this paradigm, prompting a re-evaluation of its biological relevance and the possibility that it may serve adaptive functions (Bagemihl 1999; Bailey and Zuk 2009; Richardson et al. 2024).

The growing interest in same-sex sexual behavior (SSB) has raised important questions about its causes, functions, and evolutionary implications. As reports of SSB in invertebrates continue to accumulate, long-standing assumptions in evolutionary biology and behavioral ecology are being challenged, especially given that invertebrates comprise majority of known animal species (Eisenhauer and Hines 2021). With their remarkable diversity in reproductive strategies, social systems, and sexual morphologies (Eisenhauer and Hines 2021), invertebrates offer a powerful framework for investigating sexual behavior beyond vertebrate-centered models. Nonetheless, despite their ecological and taxonomic richness, invertebrates remain underrepresented in research on non-reproductive sexual interactions, including those involving same-sex individuals.

Historically, the classical narrative in behavioral biology held that non-reproductive sexual acts were maladaptive or pathological (Ryan and Rand 1993). Early exceptions, such as male-male copulation in acanthocephalan worms (Abele and Gilchrist 1977), were treated as curiosities rather than integrated into broader evolutionary frameworks. In contrast, recent decades have seen a surge in interest and data, leading to the recognition that SSB is neither rare nor necessarily maladaptive (Scharf and Martin 2013; Monk et al. 2019; Richardson et al. 2024). This growing attention has been fueled in part by studies using controlled laboratory conditions, such as genetic mutants of Drosophila melanogaster that exhibit robust male-male courtship (Yamamoto and Nakano, 1999), and detailed behavioral observations in field and semi-natural environments, such as same-sex tandem running in termites (Reticulitermes speratus) under predator threat (Matsuura et al. 2002). These studies have moved the field beyond anecdotal observations to systematic data collection and hypothesis testing.

Currently, SSB has been documented in a wide range of invertebrate taxa. For example, male-male courtship and mounting behaviors have been found to be common in beetles (Stojković et al. 2010), crickets (Bailey et al., 2013; Boutin et al. 2016), and parasitic wasps (Benelli et al. 2013). Though less studied, SSB has also been reported in spiders and millipedes (Scharf and Martin 2013). Limpets and squids have been observed to display complex same-sex interactions, often linked to sex change or misdirected spermatophore transfer (Rivera-Ingraham et al. 2011; Hoving and Robison 2012). Flatworms, especially the genus Macrostomum, showed reciprocal copulation and hypodermic insemination between same-sex partners (Ramm et al. 2015; Schärer et al. 2017). Similarly, shrimps such as Lysmata wurdemanni display sex-change behaviors influenced by the social environment, including same-sex pairings (Baeza and Bauer 2004).

The scientific literature presents three main hypotheses to explain same-sex sexual behavior (SSB) in invertebrates: (i) mistaken identity or indiscriminate mating, (ii) social and environmental influences, and (iii) adaptive functions. The first hypothesis suggests that SSB may result from an inability to accurately distinguish sexes, especially in species with weak sexual dimorphism or under time-constrained mating conditions (Sales et al. 2018; Monk et al. 2019). For example, male crickets (Teleogryllus oceanicus) often attempt same-sex copulation in dense environments where sex-specific cues are limited (Bailey and French 2012). Similarly, hermaphroditic flatworms such as Macrostomum lignano exhibit reciprocal copulation and hypodermic insemination between same-sex partners, potentially driven by sexual conflict or strategic sperm allocation (Schärer and Ladurner 2003; Vizoso and Schärer 2007). The second hypothesis emphasizes how social structure, and environmental context can shape SSB. In species like termites and shrimps, same-sex interactions may reflect colony dynamics or responses to ecological pressures such as sex ratio imbalances, crowding, or predation (Matsuura and Nishida 2001; Baeza and Bauer 2004). Environmental disturbances, such as flooding in Calopteryx splendens, can alter mating behavior and trigger transient same-sex interactions (Gołąb and Śniegula 2012). Likewise, fungal infections have been linked to increased male-male mounting in Schistocerca gregaria, possibly due to changes in sensory processing or reproductive urgency before death (Clancy et al. 2017). The adaptive hypothesis proposes that SSB may offer direct or indirect fitness benefits (Bailey and Zuk 2009; Mizumoto et al. 2016). These may include mating practice, social dominance, stress relief, reproductive assurance in hermaphrodites, or survival advantages. For example, in the termite R. speratus, same-sex tandem running enhances group cohesion and reduces predation risk (Matsuura et al. 2002; Li et al. 2013). Such cases suggest that SSB, far from being maladaptive, can function as context-dependent and evolutionary relevant behavior. Theoretical models by Lerch and Servedio (2007) further support how indiscriminate mating can persist under high-density conditions, while Scharf and Martin (2013) emphasized the need to view SSB as part of insects’ normal behavioral spectrum.

Although SSB has been documented across numerous invertebrate taxa, its occurrence is not without potential costs. Beyond the immediate consequence of reduced reproductive output, some studies have reported additional fitness-related drawbacks. For instance, SSB has been associated with decreased lifespan in seed beetles (Acanthoscelides obtectus) and parasitic wasps (Psyttalia concolor) (Stojković et al. 2010; Benelli et al. 2013), as well as with energetic expenditures, physical harm such as genital damage in acanthocephalan worms (Abele and Gilchrist 1977), and diminished mating success due to less time allocated to courting females (Bailey et al. 2013). These findings suggest that the persistence of SSB within populations likely reflects a complex balance of costs and benefits, influenced by ecological context and selective pressures. Understanding this trade-off is essential to elucidate the evolutionary dynamics underlying SSB.

Understanding the ecological and evolutionary contexts of same-sex sexual behavior (SSB) in invertebrates requires attention to both proximate mechanisms and broader adaptive frameworks. A range of neurogenetic, chemical, and environmental factors appear to regulate SSB expression (Bailey et al. 2013; Scharf and Martin 2013; Hoskins et al. 2015; Lane et al. 2016; Mizumoto et al. 2023). In model organisms like Drosophila, genes such as fruitless and doublesex control sex-specific neuronal circuits, with mutations leading to male-male courtship (Yamamoto and Nakano 1999; Rideout et al. 2015). More recently, transcription factors like Myc have been shown to suppress such behaviors under typical conditions, revealing the behavioral plasticity that can emerge from neural perturbations (Pan et al. 2022). Chemical cues, especially cuticular hydrocarbons (CHCs), also play a central role in mate recognition among insects. Alterations in these signals can result in recognition errors and same-sex interactions (Benelli and Canale 2012; Seidelmann 2023). In some cases, SSB may even be reinforced by social experience: males that have been courted by others may show heightened mating competitiveness (Benelli et al. 2013). This raises the possibility of feedback mechanisms and social learning in sexual behavior. From an adaptive perspective, SSB has also been interpreted as a byproduct of indiscriminate mating strategies, particularly in short-lived species or high-density populations where missing a mating opportunity may be costlier than engaging in a mistaken one (Sales et al. 2018; Monk et al. 2019). Evidence from crickets (T. oceanicus) and flour beetles (Tribolium castaneum) supports this view (Bailey and French 2012; Martens et al. 2024). However, such behaviors can be condition-dependent; for instance, male crickets in poor physiological health engage less in SSB, suggesting its expression may be sensitive to individual fitness (Richardson et al. 2024). As Han and Brooks (2015) demonstrated, males engaging more often in SSB achieved higher initial success under male-biased ratios, and Gavrilets and Rice (2006) argued that some alleles promoting homosexuality in one sex may increase reproductive output in the opposite sex. This suggests that the benefit of attempting to mate with a conspecific, regardless of gender, can outweigh the costs of misidentification.

This systematic review aims to synthesize the current empirical and theoretical evidence on same-sex sexual behavior (SSB) in invertebrates, addressing existing gaps in the literature. Based on a broad range of taxa, including insects, arachnids, mollusks, annelids, and crustaceans, the study examines the prevalence, ecological contexts, proximate mechanisms, and potential evolutionary implications of SSB. This review includes both intentional same-sex interactions and those likely resulting from mistaken identity, indiscriminate mating, or socially mediated cues. This inclusive approach enables a comprehensive assessment of whether SSB arises from non-adaptive processes or may confer fitness benefits through adaptive functions. As same-sex sexual behavior dataset represents reported cases only, not true prevalence across taxa, it makes the data a bit opportunistic, and subject to strong reporting bias. Given that, some classic meta-analyses like calculating absolute prevalence or richness per order would be misleading. Accordingly, we focused on three guiding questions: i) what is the reported prevalence of SSB across ecological, behavioral, and taxonomic contexts in invertebrates?, ii) what proximate mechanisms have been identified to explain the occurrence of SSB, and how do these vary across lineages?, iii) to what extent is SSB explained by adaptive functions versus non-adaptive hypotheses, and what are the documented fitness consequences?

We systematically reviewed peer-reviewed literature (1900–2025), extracting all invertebrate SSB reports. Data included taxonomic group, sexual system, ecological context, behavioral type, and whether adaptive or non-adaptive explanations were proposed. Reviews without original data were excluded unless providing mechanistic insights.

SSB was defined based on behavioral phenotype, not sexual orientation or preference, which are often inappropriate or unmeasurable constructs in invertebrate species (Bailey and Zuk 2009; Monk et al. 2019). Relevant literature was identified using advanced searches in online databases including Web of Science, Scopus, ScienceDirect, SpringerLink, and PubMed, employing combinations of search terms such as “same-sex sexual behavior,” “homosexual behavior,” and “invertebrates” alongside specific taxonomic identifiers (i.e., “arthropods,” “mollusks,” “annelids,” “flatworms”). Studies were included if they documented observable SSB in invertebrates (defined as courtship, mounting, copulation, insemination, or pairing between individuals of the same sex). Excluded were studies lacking original behavioral data or those addressing only vertebrates. From each included study, we extracted taxonomic data (phylum, order, species), description of the SSB observed, ecological setting (laboratory, field, or semi-natural), and any proposed adaptive or non-adaptive explanations. Additionally, we recorded whether fitness consequences were investigated and categorized them as positive, negative, neutral, or unknown. Because our study involved analyzing data from previous articles, it was not possible to record data blind to minimize observation bias. However, we carried a thorough revision of published data to include only studies where data was sufficiently collected, to be properly assessed as evidence for any of the proposed hypotheses.

SSB mechanisms

To explore variation in proximate mechanisms, associations between taxonomic groups and behavioral outcome were analyzed using generalized linear models. A phylogenetic signal test (Pagel’s λ) was conducted to assess whether SSB patterns show evolutionary conservatism within lineages, using trait mapping plus a realistic phylogenetic tree topology (equal branch lengths for simplicity). About 85 orders with no described SSB were added, while 27 orders with described SSB were included in the analysis (Tab. S1 and Tab. S2).

SSB prevalence

To account for variation in taxonomic effort and known species richness among functional groups, reporting rates were standardized being divided by the number of documented SSB species in that group, multiplying by 1,000 to yield a relative reporting index. This allowed us to compare documentation density rather than raw report frequency and identify groups potentially underrepresented in the literature. Descriptive statistics were used to summarize overall frequencies and types of SSB, while bar plots and heatmaps were generated to visualize behavioral patterns by group and ecological context. To determine whether observed reporting rates were significantly associated with functional group, sexual system, or ecological context, chi-square tests of independence were applied; these were aimed at identifying whether reporting biases or ecological constraints were non-randomly distributed across taxa.

SSB hypotheses evaluation

To evaluate the extent to which ecological or biological variables predicted whether an SSB instance was interpreted as adaptive, a binomial logistic regression model using ecological context and behavioral type as predictor variables was done. This analysis addressed the question of whether adaptive interpretations were more common in certain environments or taxa. In cases where phylogenetic information was available, the presence of SSB was phylogenetically clustered using Pagel’s λ and Blomberg’s K, which helped assess whether related species were more likely to exhibit SSB due to shared ancestry. Finally, to test the robustness of observed patterns, sensitivity analyses were conducted by excluding studies with anecdotal or weakly contextualized data, allowing to verify that trends were not disproportionately shaped by a few outliers. All statistical analyses were conducted using Python (v3.10) and R (v4.3.2), and graphical visualizations were generated using the seaborn, matplotlib, and ggplot2 packages.

To strengthen the methodological framework and identify hidden patterns in SSB across invertebrate species, an unsupervised machine learning approach was performed, using KMeans clustering combined with Principal Component Analysis (PCA) for dimensionality reduction. This allowed to model latent behavioral groupings based on encoded taxonomic identity, ecological context, and SSB type. Each categorical variable was numerically encoded and subjected to clustering across the multi-dimensional space. The input features included taxonomic group, ecological context (lab, field), and SSB type (copulation, mounting, spermatophore transfer). A three-cluster KMeans model (k = 3) was selected based on visual inspection of the PCA distribution and inertia minimization.

Taxonomic Distribution and Prevalence of SSB

A total of 219 unique peer-reviewed articles and 12 reviews documenting same-sex sexual behavior (SSB) in 203 invertebrate species. The data covers a wide range of taxa including arthropods (insects, arachnids, crustaceans), mollusks (cephalopods, gastropods), annelids (polychaetes only), echinoderms (sea stars, sea urchins), and other phyla like Acanthocephala (thorny-headed worms), Nematoda, and Platyhelminthes. The publications span from 1895 to 2024, reflecting over a century of academic interest in invertebrate SSB. Within the systematic review, three hypotheses emerged as the most frequently cited to explain the occurrence of same-sex sexual behavior (SSB) in invertebrates: (i) mistaken identity or indiscriminate mating, (ii) social and environmental influences, and (iii) adaptive functions. These explanatory frameworks were present across diverse taxonomic groups (Fig. 1). For instance, the fruit fly Drosophila melanogaster and the red flour beetle T. castaneum each appeared in multiple investigations that linked to different hypotheses to explain SSB, from mistaken identity (Sales et al. 2018) to social influence (Martin et al., 2015) or indiscriminate mating (Martens et al. 2024). These repeated cases were carefully treated to avoid duplication in prevalence metrics, while still considering the variation in hypotheses and results.

SSB was most frequently reported in insects, which accounted for about 89% of the documented cases in the dataset (195 articles). This was followed by much lower reporting frequencies for mollusks, crustaceans, and arachnids. After normalizing by known species richness, the relative reporting index (RRI) revealed that mega-diverse orders like Hymenoptera and Coleoptera are, in fact, significantly underrepresented in literature (Fig. 2). Conversely, taxa such as Odonata (dragonflies), Cephalopoda (squid), and Cidaroida (pencil urchins) were highly overrepresented. While holometabolous insects had more total reports, certain hemimetabolous groups like Odonata were particularly prominent based on their high RRI. Among other groups, marine invertebrates like polychaetes and arachnids were underrepresented, while rare but notable cases were recorded in phyla such as Acanthocephala and Nematoda.

A chi-square goodness-of-fit test confirmed that the documented cases were non-randomly distributed across higher taxonomic groups, revealing a highly significant deviation from an equal distribution of reports (χ² ≈ 950, p < 0.001). This result is overwhelmingly driven by the massive number of reports in insects compared to all other groups combined. A similar test showed a significant, though less pronounced, association with ecological context, with more reports from the field than from the laboratory (χ² ≈ 57.78, p < 0.001) (Fig. 3).

Behavioral types

Common SSB behaviors observed included copulatory attempts or actual genital contact, which was the most frequently documented behavior, appearing in over half the studies and spanning numerous orders including Coleoptera, Diptera, Odonata, and Hemiptera. Courtship displays were also common, particularly in laboratory studies of Diptera, Hymenoptera, and Lepidoptera. Less frequently, mounting was explicitly recorded as a distinct behavior from copulation, alongside pair-bonding or tandem behaviors, which were noted in taxa like Isoptera (termites) and Asteroidea (sea stars). Multiple behavioral types were often recorded within a single order. While complex interactions like pairing were observed in both field (i.e., Asteroidea) and laboratory settings (i.e., Isoptera), many observations of courtship and mounting came from controlled lab studies. The data indicates that cue types vary by taxa; chemical cues such as pheromones and cuticular hydrocarbons were noted as important in insects like Hemiptera and Hymenoptera, while vibrational signals were documented in Hemiptera and chemotactic attraction was noted in Nematoda.

Ecological Context and Experimental Settings

The ecological context in which behaviors were observed is a key factor, with the majority of reports (approx. 76%) stemming from field observations, while a significant portion (approx. 24%) came from laboratory assays, few studies explicitly combined both contexts. SSB was robustly recorded in natural habitats, while laboratory studies often provided a controlled environment to investigate behaviors with clear ecological relevance, such as the anti-predator tandem running observed in Reticulitermes termites.

The vast majority of observations were in gonochoric (separate-sexed) species, where male-male interactions such as copulation, mounting, and courtship were the most frequently recorded behaviors across numerous orders. The dataset includes a few examples of hermaphroditic or sex-changing species. In these cases, observed behaviors included male-male courtship (in the shrimp L. wurdemanni), courtship displays (in the polychaete Ophryotrocha diadema), and hypodermic self-insemination (in the flatworm Macrostomum hystrix). Notably, the behaviors in some of these listed hermaphroditic species were interpreted as adaptive, such as for reproductive assurance or reducing competition (Baeza and Bauer 2004).

Where phylogenetic analyses were included, patterns varied. The wide distribution of SSB across disparate phyla and the variety of proposed hypotheses suggest that the behavior's origins are complex, likely involving both lineage-specific predispositions and convergent evolution driven by diverse ecological and social pressures. Pagel’s λ indicated strong phylogenetic signal (λ = 0.913, p < 0.001), while Blomberg’s K suggested low-to-moderate clustering (K = 0.36, p = 0.048).

SSB hypotheses testing

The most frequently cited non-adaptive explanation for SSB was "mistaken identity," which was suggested for numerous species across orders like Coleoptera, Diptera, Hemiptera, and Orthoptera, often attributed to a lack of clear sex-recognition cues. Its simile, “Indiscriminate mating”, was also frequently cited as explanation for SSB. Nevertheless, various adaptive functions were also proposed. These include SSB as a mechanism to reduce male-male competition (i.e., Gnatocerus cornutus), to practice and enhance future mating success (i.e., P. concolor), to maximize insemination opportunities in low-visibility environments (i.e., deep-sea squid), or as an anti-predator strategy (i.e., tandem running in Reticulitermes termites). Several studies indicate that high population density increases the frequency of same-sex sexual behavior (SSB). In crowded environments, recognition errors become more likely, and individuals face stronger pressure to mate quickly before losing opportunities. A chi-square test comparing sexual system and the adaptive versus non-adaptive interpretation of behaviors yielded a significant association (χ² = 4.51, p = 0.034). Logistic regression showed that behaviors in species inhabiting high-density or high-risk environments (i.e., termites under threat) were more likely to be interpreted adaptively (z = 2.21, p = 0.027). While fitness consequences were not systematically reported, specific studies indicated costs (i.e., reduced longevity in the beetle A.s obtectus), benefits (i.e., the adaptive functions listed above), or neutral effects (i.e., in the flour beetle T. castaneum).

To identify latent patterns in the occurrence of same-sex sexual behavior (SSB) across invertebrates, we applied PCA followed by KMeans clustering (k = 3). The dataset, which encoded taxonomic affiliation, ecological context (laboratory vs. field), and SSB type (i.e., copulation, mounting, spermatophore transfer), was reduced into two principal components for visualization. The analysis revealed three distinct clusters (Fig. 4). Cluster 1 contained 98 cases, Cluster 2 encompassed 70 cases, and Cluster 0 grouped 52 cases. These clusters were clearly separated in the PCA space, suggesting non-random associations among taxonomy, behavioral form, and ecological setting. Visual inspection indicated that: i) one cluster was enriched in laboratory-based reports of insects, often describing mounting or courtship under artificial density conditions; ii) a second cluster contained field observations of diverse arthropod orders, with copulation being the dominant SSB type; iii) the third cluster appeared to combine more phylogenetically distant taxa (i.e., annelids, mollusks, acanthocephalans), where SSB was typically noted as rare or incidental.

Meta-analysis from N = 22 studies reporting fitness data indicated no overall significant effect (Hedges' g = 0.103; 95% CI: -0.016 to 0.222), but subgroup analyses suggest context-dependent outcomes. Strong evidence for non-adaptive drivers was found in species with rapid mating dynamics, weak sexual dimorphism, and overlapping chemical profiles. However, even in these cases, behaviors sometimes provided secondary benefits (i.e., stimulation of later heterosexual success), blurring the adaptive versus non-adaptive dichotomy.

Same-sex sexual behavior was found to be taxonomically widespread and contextually diverse among invertebrates, although unevenly reported. Although previously considered as anomalous or maladaptive, SSB seems to serve functional roles, from reducing predation risk and enhancing mating skills to ensuring reproductive continuity in sex-limited environments. In this sense, SSB may be a form of evolutive behavioral plasticity, responding to ecological, social, or physiological pressures.

The predominance of insects and flatworms in documented cases mirrors earlier observations (Bailey and Zuk, 2009; Scharf and Martin, 2013), yet our findings reinforce this trend likely reflects research bias rather than true behavioral frequency. Insects are frequently used in behavioral and genetic experiments due to ease of laboratory rearing, while flatworms, particularly the genus Macrostomum, offer transparent bodies and observable reproductive traits that facilitate experimental observation (Schärer et al. 2017).

The significant chi-square result indicating a non-random taxonomic distribution of SSB reinforces concerns raised by Rivera-Ingraham et al. (2011) and Monk et al. (2019), who highlighted the neglect of lesser-studied marine and benthic taxa. Our standardized reporting metric helps adjust for research effort but cannot fully disentangle discovery bias from true absence of behavior. Future field surveys in underrepresented clades, such as polychaetes or echinoderms, may reveal a broader spectrum of SSB than is currently acknowledged.

Ecological context showed influence on the type and interpretation of SSB. Our results confirm that laboratory environments disproportionately document behaviors such as mounting and courtship, particularly in species like D. melanogaster and T. castaneum. While controlled settings allow for standardized comparisons, they may also elicit behaviors that are rare or absent under natural conditions. This artificial inflation of certain behaviors has previously been critiqued (Bailey et al. 2013; Clancy et al. 2017), and our results corroborate those concerns by highlighting a higher frequency of maladaptive interpretations in laboratory studies. Conversely, field-based reports often document SSB behaviors with presumed non-adaptive or environmentally constrained origins, such as mistaken spermatophore implantation in Octopoteuthis deletron (Hoving and Robison 2012) or tandem pairing in C. splendens following flooding events (Gołąb and Śniegula 2012). These behaviors may result from temporary disruptions in sensory cues, population density, or predator-induced stress, underscoring the need to account for ecological variability when interpreting SSB.

Sexual systems seem to shape SSB patterns. Hermaphroditic species such as M. lignano and L. wurdemanni frequently engage in reciprocal copulation and show high rates of adaptive interpretations, supporting the idea that flexible sex allocation strategies can promote the evolution of SSB (Schärer and Ladurner 2003; Baeza and Bauer 2004). The chi-square results corroborate that hermaphroditism is significantly associated with adaptive framing of SSB, echoing findings from Ramm et al. (2015), who argued that reproductive assurance, sperm competition, and social learning may all shape these behaviors. In contrast, gonochoric species, particularly insects, often exhibit unilateral SSB behaviors interpreted as mistaken identity, especially in crowded conditions or in the absence of sex-specific cues (Bailey and French 2012; Sales et al. 2018). This aligns with our regression results showing that ecological complexity, more than taxonomy or sexual system alone, predicts the likelihood of an adaptive explanation. These findings provide support for the hypothesis that SSB may emerge as a context-dependent trait modulated by external pressures rather than a fixed behavioral syndrome. In fact, under environmental stress or predator pressure, organisms may reduce the time spent on sexual discrimination, favoring indiscriminate behaviors such as rapid mounting with same-sex partners. Similarly, laboratory conditions, where densities are artificially high and environmental cues are reduced, have also been reported to exacerbate the occurrence of SSB.

The phylogenetic signal detected by both Pagel’s λ and Blomberg’s K suggests a strong level of evolutionary conservatism in the presence of SSB, paralleling observations in vertebrate systems (Monk et al. 2019). This reinforces the conclusion that the occurrence of Same-Sex Behavior (SSB) in invertebrates shows a significant phylogenetic signal, being not randomly scattered across the invertebrate tree of life; instead, clustering within related lineages. The last suggests that both shared ancestry and convergent ecological pressures contribute to the occurrence of SSB. This nuanced view challenges earlier models that treated SSB either as entirely maladaptive (Abele and Gilchrist 1977) or solely as a byproduct of indiscriminate mating (Han and Brooks 2015). Instead, our findings suggest that SSB may represent a flexible evolutionary response shaped by lineage history and immediate social or environmental conditions. However, it must be considered that this analysis is based on reported cases, therefore, the absence of SSB in the 85 control orders is, more accurately, an absence of evidence, not necessarily evidence of absence, reflecting human research effort more than the complete distribution of animal behavior. In fact, some invertebrate groups, like fruit flies, certain beetles, and commercially relevant butterflies, are studied intensively. Their behaviors, including SSB, are well-documented, while countless other orders are cryptic, difficult to culture, live in inaccessible environments or are simply not a focus of research funding. SSB could be common in these groups but entirely unobserved. Still, even with these significant data limitations, the strong phylogenetic signal is still a very meaningful result. Instead of searching randomly, researchers can now target their efforts. Future research should focus on sister groups to the major insect orders with high rates of SSB.

The unsupervised machine learning analysis provides a novel contribution to the study of animal behavior. The use of KMeans clustering, supported by PCA, revealed three distinct behavioral groupings not fully predicted by taxonomy alone. These clusters reflected: i) experimentally tractable species showing copulatory behaviors under artificial conditions, ii) adaptive reciprocators such as hermaphrodites, and iii) naturally observed species with low-frequency or error-driven behaviors. This typology aligns with frameworks proposed by Scharf and Martin (2013) and Lane et al. (2016) but provides a data-driven method for classification. The integration of artificial intelligence tools into behavioral ecology is still at an early stage. However, our results show that even basic unsupervised models can uncover meaningful patterns that enhance or even challenge expert-based classifications. Future studies could employ neural networks or ensemble models incorporating ethological metadata to refine predictions of when and where SSB is likely to evolve. This approach has the potential to revolutionize comparative behavior studies by increasing objectivity and expanding analytical scalability.

Although non-adaptive hypotheses such as mistaken identity or indiscriminate mating have often been invoked to explain SSB, these mechanisms may themselves represent adaptive strategies. In certain contexts, the benefit of attempting to mate with a conspecific may exceed the costs of a misidentification, as has been proposed by Han and Brook (2015) and Gavrilets and Rice (2015). This perspective helps to explain why same-sex interactions are observed across such a wide diversity of invertebrate taxa, despite the potential fitness costs associated with injuries, wasted gametes, or reduced longevity. By reducing the risk of lost reproductive chances, these behaviors may provide a selective advantage that contributes to their persistence across evolutionary lineages.

This study provides a comprehensive quantitative synthesis to date of SSB in invertebrates, spanning over four decades of research and applying both classical statistics and machine learning. In doing so, it helps bridge persistent gaps in our understanding of how sexual behavior evolves outside the vertebrate-centric framework. Our results support the growing consensus that SSB is not inherently maladaptive but may arise through diverse, often context-specific mechanisms (Bailey and Zuk, 2009; Mizumoto et al., 2016). Moreover, the findings reinforce the need for more inclusive and ecologically realistic studies of animal sexual behavior. With invertebrates comprising most of the animal diversity, continued neglect of these taxa limits the scope of evolutionary theory itself.

Funding declaration

This study was funded by the Programa de Apoyo a la Instalación en Investigación PA_INST_2025_25 to VPO, and by the ANID Scholarship Program 2023-21230929 to CMM.

Competing interests

The authors have no relevant financial or non-financial interests to disclose.

Significance Statement

Same-sex sexual behavior (SSB) has traditionally been viewed as anomalous or maladaptive. Our systematic synthesis across more than 200 invertebrate species demonstrates that SSB is taxonomically widespread and strongly influenced by ecological and social contexts. By integrating statistical analyses, phylogenetic signal tests, and machine learning clustering, we reveal that SSB seems to not be a random occurrence but a structured and context-dependent aspect of reproductive strategies. Evidence shows both adaptive and non-adaptive components, including benefits such as reproductive assurance, predator avoidance, and enhanced mating competence, alongside potential costs like reduced longevity. These findings underscore that SSB is not merely a byproduct of recognition errors but can serve meaningful evolutionary functions. By expanding the empirical and theoretical framework to include invertebrates, this study contributes to a broader, more inclusive understanding of sexual behavior and its evolutionary significance.

Data availability statement

All data generated or analyzed during this study are included in this published article and in the supplementary materials.

Author contributions

VPO: concept and writing of the first draft, plus the main analyses. VPO and CMM: final writing. All authors reviewed and edited the manuscript and agreed on the final version.

Ethics approval statement

Formal ethics approval was not necessary for this study.

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Same-Sex Sexual Behavior in invertebrates is widespread and context-dependent: insights from a Systematic Synthesis

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Abstract

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Introduction

Methods

SSB mechanisms

SSB prevalence

SSB hypotheses evaluation

Results

Taxonomic Distribution and Prevalence of SSB

Behavioral types

Ecological Context and Experimental Settings

SSB hypotheses testing

Discussion

Declarations

References

Additional Declarations

Supplementary Files

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Version 1